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   Sex Life Of Figs: Coevolution Of A Tree & Minute Wasp (Part 1)     Part 2  
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It is Difficult to Generalize About Fig Biology Because Of All The Exceptions
Table Of Contents For Parts 1 & 2
  1.    Brief Introduction To The Biology Of Figs
  2.    The Rustyleaf Fig & Its Pollinator Wasp
  3.    Life Cycle Of Common Fig (Ficus carica)
  4.    Important Definitions Used In Fig Biology
  5.    Roles Of Male Wasps In Fig Life Cycle
  6.    Discrepency In Monoecious Style Length
  7.    Annual Crops Of Edible Fig Syconia
  8.    Persistent vs. Caducous Fig Syconia
  9.    F. pseudocarica - F. palmata Controversy
10.    Sex Determination In Trees Of Ficus carica
11.    Calimyrna Orchards In San Joaquin Valley
12.    Drupelets: True Botanical Fruits Of A Fig
13.    Overwintering Mamme Crop Of A Caprifig
14.    Why Female Wasp Can't Oviposit In Edible Fig
15.    Vicarious Selection: Coevolution Of Fig & Wasp
16.    Parthenocapic Varieties Of Ficus carica
17.    Dangers Facing Emerging Female Fig Wasps
18.    Which Figs Grew In The Ancient Holy Land?
19.    Fossil Fig Syconia In Wyoming & Montana?
20.    Links To Articles About Figs On Wayne's Word
21.    Reference Articles Cited In Wayne's Fig Articles 
22.    Fig Species In Palomar College Arboretum
23.    Unusual Ficus dammaropsis Of New Guinea
24.    Additional Figs In Palomar College Arboretum

The distribution of 830 species of Ficus are shown in the green area of above map. Figs occur throughout the Old and New World tropics, extending north to the eastern Mediterranean and China. By far the majority of species are evergreen. The common fig (Ficus carica) is deciduous and grows in colder climates of Turkey and the Middle East. With the exception of the Hawaiian Islands, practically every tropical continent and major island group has one or more species of indigenous fig. In fact, the tiny island of Barro Colorado in the Panama Canal Zone, with an area of only six square miles, has 17 native species. Virtually every species of fig has its own unique species of "in house" wasp pollinator. The wasps are housed throughout the year inside the fig's hollow syconia, in one of nature's most remarkable symbiotic relationaships between a tree and an insect. The symbiotic wasps undoubtedly play a major role in the ability of different fig species to grow in the same locality, a phenomenon known as "species packing."

1. A Brief Introduction To The Biology Of Figs

In the late 1960s, many of the old brick buildings on the campus of Palomar College were covered with creeping fig (Ficus pumila), giving the campus a beautiful ivy-league appearance resembling the Engish ivy (Hedera helix) that covers walls and buildings of universities in the eastern United States. I began studying figs at that time, and after 40 years of teaching botany classes, I have concluded that the figs are the most remarkable trees on earth. The Plant List of Kew and Missoutri Botanical Garden (2011) gives 830 accepted species of Ficus, and they all have their own in-house pollinator wasp. Most species are evergreen and occur in rain forests throughout the tropics. They are a major factor in tropical ecosystems, providing sweet fruits for numerous animals, including parrots, hornbills, toucans and monkeys. Fruit-eating bats commonly disperse the seeds in their excrement, and seedlings often start out as epiphytes on branches high in the rain-soaked canopy. The common edible fig (F. carica) is deciduous and extends north into temperate regions of Europe and the Middle East. The many uses of figs by people is legendary, and there is good evidence that the common fig was one of the earliest cultivated trees. Depending on the reference, there are an estimated 400+ cultivated varieties of the common fig.

  Kew List Of Plant Species: www.theplantlist.org/  

The creeping fig (Ficus pumila) of eastern Asia. There are two distinct types of stem growth: Young, juvenile branches and older, mature branches. The juvenile branches with smaller leaves (top) produce aerial roots that adhere to concrete, stucco, masonry and even glass windows. Without pruning, a single plant can envelop a four-story building. The syconium is lined with all long-style female flowers. Without pollen-bearing male plants and fig wasps, no seeds can be produced and this plant must be propagated by cuttings. In its native habitat there are also male plants (caprifigs) with male flowers and wasp-bearing female flowers. When I began teaching at Palomar College in the late 1960s, this fig covered many of the old brick buildings. The campus truly had an "ivy-league" appearance, except our "ivy" was the creeping fig. The new growth had to be constantly trimmed around windows and doors, and eventually all the plants were removed by the gardening staff.

Creeping fig (Ficus pumila): Close-up view of the aerial roots (red arrow) that develop at the nodes on juvenile branches. The aerial roots secrete a clear, gummy latex that works like rubber cement. The roots adhere to concrete, masonry and glass. This remarkable adhesive was first described in detail by Charles Darwin in his book The Movements and Habits of Climbing Plants (1876). Older, mature branches with larger leaves produce flower-bearing syconia. This species is commonly planted in southern California to cover the monotanous concrete walls of buildings and freeways. In fact, it was been crossed with the edible fig (F. carica) to produce a hybrid vine (F. x pumila-carica). Unfortunately, the hybrid produces inedible syconia and lacks the adhesive aerial root pads. The hybrid is a sprawling vine that can grow on fences but cannot cling to vertical concrete walls like its F. pumila parent (see next image).

Ficus x pumila-carica: A hybrid between the creeping fig (Ficus pumila) and the common edible fig (F. carica). It has leaves and syconia intermediate between the parents; however, the syconia are basically inedible compared with F. carica. In addition, the hybrid lacks the adhesive aerial roots of F. pumila.


2. Rustyleaf Fig (Ficus rubiginosa) & Its Remarkable Pollinator Wasp

All figs rely on tiny symbiotic wasps for their pollination. Minute male and female fig wasps are borne inside hollow, fleshy, flower-bearing structures called syconia. The syconium is what most people associate with the tasty fruit of a fig, but technically it is not a true fruit. The syconium is lined on the inside with hundreds of tiny male and female flowers. The flowers are greatly reduced and do not have petals. Male flowers consist of pollen-bearing anthers. Female flowers are of two types: Long-style, seed-bearing flowers and short-style flowers that bear fig wasps instead of seeds. Wasp eggs are not laid in the ovaries of long-style flowers because the wasp's ovipositor cannot reach the ovary.

A. Close-up view of a male and female fig wasp (Pleistodontes imperialis) that inhabits the syconia of the Australian rustyleaf fig (Ficus rubiginosa). The slender ovipositor on female wasp is too short to penetrate the ovary of long-style flowers; therefore she does not lay eggs in these flowers. The smaller, wingless male has large mandibles and a greatly reduced body which has two primary purposes: (1) Inseminating the female and (2) Chewing exit tunnels through the syconium wall through which the females escape. The "eye" of an ordinary sewing needle is shown for a size comparison. These wasps were collected from trees growing by the old Life Science building. The biology students were always amazed when I brought them into my laboratory classes.

B. A non-pollinator "bogus" fig wasp collected from the syconium of the Baja California wild fig (Ficus palmeri, or possibly Ficus brandegeei). The ovipositor is much longer than the symbiotic pollinator wasp. In fact, some non-pollinator wasps can penetrate the entire syconium wall from the outside. Non-pollinators can also lay eggs in long-style fig flowers reserved for fig seeds. Consequently, no seeds are produced in these flowers. In addition, these "bogus" fig wasps do not pollinate fig flowers. Although they do not benefit the fig tree, non-pollinator wasps of the families Torymidae and Eurytomidae are common inhabitants of New World monoecious fig syconia. Their coexistence with natural fig pollinator wasps is a complex and perplexing coevolutionary problem in fig biology.

  Size Of Sewing Needle In Wayne's Word Images  
Ficus palmeri In Mtns & Coastal Baja California

Fig species have one or more pollinator wasps in the family Agaonidae that enter their syconia through a small opening called an ostiole to pollinate the female flowers inside. Although pollinator wasps are often host specific, one pollinator can have more than one host (J.M. Cook and J.-Y. Rasplus, 2003). In addition, the syconium may contain one or more non-pollinating wasps in a different wasp families. Like the pollinator wasps, the nonpollinators have flattened heads and bodies, and are perfectly adapted to squeeze between the ostiolar bracts of receptive syconia. This is yet another example of convergent evolution. Without the pollinator wasps transferring pollen from one syconium to another, the female flowers inside would not get pollinated and no seeds would be produced (a catastrophe for the fig tree). In the common edible fig (Ficus carica), the female wasp gets covered with pollen as she exits the male caprifig. In many tropical fig species, the wasp packs her pollen baskets (corbiculae) on the underside of her thorax before leaving the syconium. When she enters another receptive syconium, she transfers her load of pollen to the female flowers inside. I have observed this latter scenario many times on rustyleaf figs on campus. Unfortunately, most of these trees were cut down to make room for new buildings. Hopefully, some of these wasps have made their way to the Arboretum.

A 34 million-year-old fossil fig wasp from the Eocene was dicovered in limestone on the Isle of Wight, England (Stephen Compton et al. 2010). It was originally thought to be a tiny winged ant, but was later confirmed to be a female fig wasp because of the pair of pollen baskets (corbiculae) on the underside of its thorax. The corbiculae of this wasp named Ponera minuta even contained Ficus pollen. The previous record for ancient fig wasps was 23 million-year-old Dominican Republic amber from the Miocene. DNA phylogenetic analysis indicates that the fig and fig wasp relationship may extend back more than 65 million years ago to the Cretaceous Period. The Isle of Wight fig wasp is relatively unchanged compared with present-day fig wasps of the family Agaonidae. "No innovations in the relationship are discernible for the last tens of millions of years." According to Nefdt and Compton (1996) short-style female flowers in moneous figs have longer styles than those in male figs of dioecius species. The shorter ovipositor of Ponera minuta indicates that its symbiotic host was dioecious, an advanced reproductive pattern in fig evolution.

Fossil leaves embedded in 60 million-year-old limestone from the Fort Union Formation near Glendive, Montana have tentatively been identified as Ficus. Fossil fig syconia named Ficus ceratops from the 70 million-year-old Hell Creek Formation in this area have been clearly shown to be a different species, possibly an extinct palm. See Section 17 on this page: Fossil Fig Syconia in Wyoming and Montana.


3. Life Cycle Of The Common Fig (Ficus carica).

Life cycle of the common fig (Ficus carica). Style length is genetically determined and it is vital that syconia on seed-bearing female trees have styles longer than the female wasp's ovipositor. Unable to reach the ovaries of these flowers, she does not lay eggs (oviposit). Therefore, a seed develops inside the ovary rather than a hungry wasp larva. She can only oviposit in the short-style female flowers on "male" trees called caprifigs. Caprifig trees produce pollen and the crucial pollinator wasps (Blastophaga psenes). In some common figs termed "caducous" or early deciduous, the immature female syconium drops from the tree if the flowers inside are not pollinated. There are many cultivated "parthenocarpic" varities of the common fig in which the syconia develop on female trees wthout wasp pollination (caprification). The ripe syconia are fleshy and edible; however, the numerous ovaries (drupelets) inside are hollow and seedless.


4. Some Definitions Used In Fig Biology

Style Length-Ovipositor Length Hypothesis: This refers to oviposition through style of female flower by pollinator wasp. Wasp ovipositor can penetrate ovary of short-style flower where egg is deposited. Ovipositor is too short to penetrate ovary of long-style flower. Consequently, wasp larvae occupy ovaries of short-style flowers while seeds develop in ovaries of long-style flowers. This mechanism limits seed predation in dioecious figs, but may not hold true in most monoecious figs.

Hypotheses For Limiting Seed Predation In Monoecious Figs:

  1. Stigma morphology controlling preferential oviposition.
  2. Aborting syconia with too many parasitized seeds.
  3. Limiting number of pollen-bearing wasps through ostiole.
  4. More ovaries in syconium than wasp can oviposit in.
  5. Short life span of pollen-bearing female wasps (foundresses).
Gall Flower = Short-style Female Flower: Oviposition and the presence of a wasp larva initiates the development of endosperm tissue that the larva feeds on. Since pollination is not required, the developing wasp-bearing ovary is called a gall. This relationship is clearly seen in the ovaries of Ficus sycomorus inhabited by the nonpollinator wasp Sycophaga sycomori. It is also seen in the overwintering mamme crop of F. carica caprifigs where developing wasp larvae feed on endosperm tissue from unpollinated flowers in the previous mammoni crop. According to some fig biologists, since the normal course of events is to abort unpollinated syconia in caducous figs, the entire syconium could be viewed as a gall occupied by nonpollinator wasps. [Some fig biologists also state that the short-style flower is pollinated and the larva feeds on the endosperm of developing seed.] According to Storey (1977) the term "gall flower" is a misomer because it is fully capable of producing normal seed-bearing drupelets if pollinated, and in this respect are no different from long-style flowers.

  Gall Flowers In Figs  

Foundress: Gravid, pollen-bearing female pollinator wasp that enters ostiole of specific syconium during receptive stage.

Parthenocarpy: Development of the ovary of a flower without pollination and fertilization. In figs, this refers to the hollow, seedless druplets (cenocarps). In figs the outer syconium also develops.

Stimulative Parthenocarpy: Development of the drupelet by the oviposition and habitation of wasp larva. Since the egg and embryo sac is destroyed in the process, the nutritive nucellar and endosperm tissue that the larva feeds on develops without fertilization. The resulting druplet is a hollow psenocarp bearing a wasp larva.

Vegetative Parthenocarpy: Development of drupelets and syconium without pollination, fertilization or any known stimulus. The druplets are hollow cenocarps. This is characteristic of common figs with the persistent gene. These figs do not require pollination by a fig wasp (caprification); however, they are fully capable of producing seed-bearing drupelets if they are pollinated and fertilized.

Parthenogenesis: Development of the egg into an embryo without fertilization. This also applies to the development of endosperm tissue without fertilization of the two polar nuclei within the binucleate endosperm mother cell. Parthenogenetic endosperm tissue in figs has the same chromosome number as sporophtye tissue (2n = 26) according to Saleeb (1965).

  Apomixis: Parthenogenesis & Agamospermy  

Syconium: An inside-out inflorescence composed of a hollow, fleshy structure (peduncular tissue) lined on the inside with hundreds of tiny unisexual, apetalous flowers. Some authors state that it is composed of receptacle tissue, but Storey (1977) states that this is incorrect. Some authors refer to the syconium as a compound or multiple fruit because it contains many ripened ovaries derivied from many separate flowers. The actual fruits of a fig are the one-seeded drupelets that form inside wasp-pollinated syconia.

Drupelet: The actual fruit from the ovary of a long-style female flower, composed of a sclerified endocarp surrounding the seed. It is erroneously called an "achene." An empty druplet which develops parthenocarpically (without fertilization) is called a Cenocarp. A wasp-bearing drupe in the caprifig is called a Psenocarp.

Protogynous: Female flowers are receptive before male flowers mature and shed pollen. This strategy favors cross pollination and is typical of monoecious fig syconia and "male" syconia of dioecious figs.

Caprification: Pollination of a female fig (Ficus carica) by fig wasps in order to produce mature seed-bearing syconia. Without pollination, Smyrna-type (caducous) syconia will fall from the tree without ripening.

Monoecious: Fig species with pollen-bearing male flowers, short-style female flowers and long-style female flowers in the same syconia. This includes about half of the world's fig species, the other half being dioecious with separate male and female trees. Measurements of styles and pollinator ovipositors show that most ovules in most monoecious species are within the wasp's reach (Herre, andér and Macado, 2008). This significant revelation indicates that other mechanisms are involved in the determination of seed-bearing and wasp-bearing ovaries. This is quite different from Ficus carica and other dioecious species. Monoecious figs are considered to be the ancestral breeding system, dating back at least to late Cretaceous (70 million years ago) to the time of T-Rex. Again, it is extremely difficult to generalize about fig biology because of all the exceptions.

Gynodioecious: Fig species with male and female trees in the population. Male trees (caprifigs) bear "male" syconia containing pollen-bearing male flowers and short-style female flowers. The ovaries of short-style female flowers often contain a male or female wasp larva if eggs were oviposited inside them. Female trees only bear female syconia containing seed-bearing long-style female flowers and no male flowers. About half the world's 830 fig species are gynodioecious, the other half being monoecious with male flowers, short-style and long-style female flowers in the same syconium (i.e. without separate male and female trees).

Pollen Basket (Pollen Pocket) = Corbicula: A specially-adapted cavity often surrounded by fringe of hairs on underside of thorax or base of leg on female wasps where pollen is purposely deposited before exiting the syconium of monoecious and gynodioecious figs.

Coxal Comb: A specially-adapted fringe of hairs on the fore coxae (base of front legs) on female wasps. It is used to actively (purposely) gather pollen from within the syconium and store it in thoracic pockets (pollen pockets). According to Cook, et al. 2004, the presence of coxal combs always indicate active (purposive) pollination behavior, whereas pollen pockets provide a good but imperfect index. Active pollination includes serveral identifiable components: Wasps must collect pollen from anthers, place it into pockets, and deposit it onto receptive flowers. To accomplish this they require coxal combs and pollen pockets. The following paragraph from Cook, et al (2004) illustrates the complexity of pollination behavior, especially Pleistodontes froggatti in the Moreton Bay fig (Ficus macrophylla):

    "Kjellberg et al. (2001) observed pollen deposition behaviour for several species from various fig wasp genera and identified a morphological trait (presence of coxal combs) that always indicated active pollination. This trait is easy to observe and allows inference of behaviour for a much wider set of species than can be observed in the act of pollination. The presence of pollen pockets also generally indicates active pollination, but there are exceptions involving passive species in a genus that is primarily active (Kjellberg et al., 2001). The genus Pleistodontes contains the only species highlighted as a possible exception to the striking general pattern of fig pollinator coadaptation. Ficus macrophylla Desf. ex Pers. has a high anther/ovule ratio, typical of a passively pollinated fig. However, its pollinator, Pleistodontes froggatti Mayr, although lacking coxal combs (suggesting passive pollination), has pollen pockets that can contain concentrated pollen (suggesting active pollination). On balance, this species has been considered an active pollinator in two previous studies (Kjellberg et al., 2001; Jousselin et al., 2003)."
  Pollination Behavior In Different Wasp Genera  

A deceased female fig wasp (Pleistodontes imperialis) extracted from the ostiole of Ficus rubiginosa. Note the coxal comb at the base of front leg that it used to actively gather pollen from syconium and store it in ventral thoracic pocket (pollen pocket). Inset (left): SEM from Kjellberg, F., Jousselin, E., Bronstein, J.L., Patel, A., Yokoyama, J., and J.-Y. Rasplus. 2001. "Pollination Mode in Fig Wasps: The Predictive Power of Correlated Traits." Proceedings of the Royal Society of London 268: 1113-1121.

Syconium of Moreton Bay fig (Ficus macrocarpa) in Palomar College Arboretum. Palomar College horticulturist Tony Rangel grew viable seeds from this tree, so I suspected that the pollinator wasp (Pleistodontes froggatti) must be present.

Unlike the similar P. imperialis of rustyleaf figs (F. rubiginosa), P. froggatti does not have a coxal comb at the base of its front legs. According to Cook, J.M. et al. (2004), the lack coxal combs indicates passive rather than active (purposive) pollination; however, they also state that "pollen pockets provide a good but imperfect index." In Table 1 of their article they state that pollination by P. froggatti is passive. Prior to my discovery of P. froggatti in the Moreton Bay fig at Palomar College (December 2011), the only fig wasps I have documented on campus are P. imperialis on rustyleaf figs and Eupristina verticillata on the Indian laurel fig (Ficus microcarpa).

Pleistodontes froggatti from Moreton Bay fig syconium in Palomar College Arboretum.

Eupristina (Parapristina) verticillata from Indian laurel fig (Ficus microcarpa) syconia on Palomar College campus. One wasp is squeezing through an exit tunnel cut by male wasps (white arrow). Another Fig/Fig Wasp Discrepancy: J.T. Otero and J.D. Ackerman (2002) statistically analyzed the style length of native F. citrifolia and introduced F. microcarpa in Puerto Rico. They found no correlation between style length and seed predation in syconia of these trees: "Neither Ficus species showed significant differences in style length between flowers with wasps and flowers with seeds, as expected under the short-ovipositor-length hypothesis."

It is interesting to speculate on how these symbiotic wasp species were introduced at Palomar College. Were wasp-bearing syconia already present on the original plantings, or were wasps carried here by the wind from trees in neighboring cities? The Moreton Bay fig is native to eastern Australia where it grows in the rain forest and often starts out as an epiphytic vine that develops into a strangler fig. Eventually it shades out and kills its host, becoming a massive tree with a buttressed trunk and huge spreading surface roots. In Hawaii and northern New Zealand it has become naturalized because of the introduction of its pollinator wasp (Pleistodontes froggatti). In Hawaii the wasp was deliberately introduced in 1921. In New Zealand it was first recorded in 1993, having apparently arrived by long-distance dispersal from Australia, a 3,000 km (1900 mile) journey. According to R.O. Gardner and J.W. Early (1996), adult female wasps usually live 2-3 days; there are an average of 21 days over the course of a year during which the wasps could make this trip in 1-3 days on air currents. Fig wasps have been caught in light traps aboard ships up to 99 km (60 miles) offshore in the Pacific (J.C. Harrell and E. Holzapfel, 1966). Ahmed, at al. (2009) reported pollen transfer by the African fig wasp Ceratostolen arabicus between known host trees of Ficus sycomorus separated by a distance of 160 km (100 miles). Based on these records for long distance dispersal, reaching Palomar College in San Marcos from known wasp-bearing trees in coastal San Diego County is certainly plausible. Once in the vicinity of host trees, they are attracted to the correct syconia by mixtures of species-specific chemical attractants, including volatile terpenoids. For example, receptive syconia of F. hispida release blends of three fragrant monoterpenes, including linalool (major constituent), limonene and pinene (C. Chen and Q. Song, 2008).

A single large monoecious fig tree or gynodioecious "male" tree produces several crops of syconia per year. Depending on the species, one crop may consist of hundreds or even thousands of syconia, each bearing a hundred or more pollinator wasps. A large tree, such as the Moreton Bay fig could theoretically release thousands of pollinator wasps into the wind. In fact, during wasp exodus season in Balboa Park, hundreds of fig wasps from nearby trees collect in windows at the San Diego Natural History Museum!

The introduction of symbiotic fig wasps poses a serious problem of invasive strangler figs in tropical regions because of the prolific production of syconia and viable seeds. According to Jennifer Possley, Field Biologist at Fairchild Tropical Botanic Garden, five species of strangler and banyan figs are naturalized in southern Florida, including Ficus altissima, F. benghalensis, F. benjamina, F. microcarpa and F. religiosa. Throughout Key West, seeds of the Indian laurel fig (F. microcarpa) germinate readily in cracks and crevices of old buildings, gradually sending a weblike mass of aerial roots down the walls to the ground. Some residents of the Coral Gables area consider the Asiatic banyan-type figs to be a nuisance and potential menace. The massive, spreading roots of these enormous trees buckle pavement and concrete swimming pools, plug drainage and sewer lines, and pose a serious threat to underground utilities. In other parts of the world alien figs can also invade native rain forest and other plant communities. It should also be noted here that southern Florida and the Caribbean region also have native strangler figs, including F. aurea and F. citrifolia.

Naturalized figs in the Florida Keys. Strangler figs and banyans need viable seeds and a moist climate to be naturalized. Viable seeds require pollinator wasps in their syconia.

  Strangler Figs and Banyans  
Wayne's Word Fig License Plate


Topocentric Pollination: Passive mode where pollen is trapped in intersegmental folds (grooves) as wasps exit the syconium, and is rubbed off as wasps move about on stigmatic platform (synstigma) of new receptive syconium.

Ethodynamic Pollination: Deliberate (purposive) pollen transfer from pollen baskets (corbiculae) to dense stigmas of receptive female flowers (synstigma).


5. Roles Of Male & Female Wasps In Life Cycles Of Common Fig & Rustyleaf Fig

The male & female wasps in above image are Blastophaga psenes from Ficus carica. The exit tunnels were made by male Pleistodontes imperialis in the syconium wall of the rustyleaf fig (F. rubiginosa). Blastophaga males do not cut the exit tunnels through the syconium wall. Instead, the females exit through the ostiole, becoming dusted by pollen from male flowers near the ostiolar end of the syconium.

Patterns Of Collecting Pollen & Exiting Syconium By Female Fig Wasp

Pollen Collection
By Female Wasp
Female Wasps Exit
Through Ostiole
Females Exit Through
Tunnels Cut By Males
Without Pollen Baskets:
Pollen Is Carried In Grooves
Between Abdominal Segments
Passively Dusted With
Pollen From Male Flowers

Some Gynodioecious spp.
e.g. F. carica
Passively Dusted With
Pollen From Male Flowers

Some Gynodioecious spp.
  With Pollen Baskets
(Coxal/Sternal Corbiculae)
  Purposely Packs
Her Pollen Baskets

Some Gynodioecious spp.
  Purposely Packs
Her Pollen Baskets*

Monoecious & Gynodioecious
e.g. F. rubiginosa

* Common Pattern That Fits "Vicarious Selection" Example In Chapter 10 of Richard Dawkin's Climbing Mount Improbable.

  Key To Subgroups Of Gynodioecious Figs  


6. Discrepency In Style Length Hypothesis For Monoecious Figs

According to Carole Kerdelhué and Jean-Yves Rasplus (Oikos Vol. 77: 163-166, 1996), monoecious syconia of Ficus sur contain long-style and short-style female flowers densely packed together in a layer that lines the inner cavity of the syconium. Although the styles all form a relatively continuous stigmatic layer called a synstigma (i.e. all stigmas in the same plane) within the syconium, the ovaries may be deep or shallow relative to the synstigma depending on the length of their flower stalks (pedicels). Generally, the deep-seated ovaries (on short pedicels) with long styles each contain a seed, while the shallow ovaries (on long pedicels) with short styles each contain a wasp larva. A pollinator wasp walking on this "bed" of styles (synstigma) can insert her ovipositor down the short style and easily penetrate the ovary where she lays an egg. The deep-seated, long-style ovaries are out of reach for her ovipositor (style longer than her ovipositor), and consequently these ovaries develop seeds rather than wasp larvae. Because of intermediate style lengths (between long and short) and different ovary heights due to the length of flower stalks (pedicels), the ovary position of female flowers in monoecious fig syconia often forms a stratification. There are at least 4 different ovary layers occupied by beneficial (pollinator) and non-beneficial and/or harmful non-pollinator wasps. These layers are shown by different colors in the following illustration according to their position (depth) from the stigmatic surface (synstigma) within the syconial cavity.

According to Kerdelhué and Rasplus (1996), dioecious figs may have evolved from monoecious ancestral fig species due to selection pressure by non-pollinator fig wasps. Although these non-pollinator wasps belong to the same Order Chalcidoidea as pollinators, many of them belong to different families. They do not benefit the fig and may even be harmful--especially when they compete with and/or parasitize the beneficial pollinator wasps.

Monoecious Figs
     Stratified Syconium: 4 Ovary Positions     
Gynodioecious Figs
     2 Synconia Ea. With 1 Ovary Position     
  Contain (Harbor) more species of competing &  
parasitic nonpollinators. Disadvantage to fig.
  1 ovary position per syconium. Contain fewer  
species of nonpollinators. Advantage to fig.

Heterostyly and four ovary layers (stratification) within the syconium of a monoecious fig (Ficus sur). (1) Yellow: The most shallow ovaries (near surface) with shortest styles which typically contain a pollinator wasp larva; (2) Green and (3) Red: Slightly deeper ovaries that typically contain non-pollinator wasp larvae; (4) Black: The deepest ovaries with longest styles that typically bear mature seeds.
Exception to above illustration: Measurements of styles and pollinator ovipositors show that most
ovules in most monoecious species are within the wasp's reach (Herre, Andér and Machado, 2008).


7. Annual Crops Of Edible Fig Ficus carica syconia

Sex of Tree
Mature Crops Of Syconia Per Year
Male Caprifig
Profichi (June) *
Mammoni (Fall)
Mamme (Winter)
Female Tree
1st or Breba (Summer)
2nd or Main (Late Summer-Fall)

* Only the caprifig Profichi crop produces pollen, and this is used to pollinate
   the receptive main crop in June by the action of winged female fig wasps.

Female Trees:
1-2 Crops/Year

Male Trees:
3 Crops/Year

Type Of Gynodioecious Fig Cultivar Based On Sex & Whether
It Needs Caprification (Pollination) In Order To Set Fruit Crop
Unisexual Female Tree (No Male Flowers)
Syconia Contain Long-Style Female Flowers
Male Tree
(Bisexual)
Seasonal
Crop Name
Smyrna
(Caducous)
San Pedro *
(Intermediate)
Common **
(Persistent)
Caprifig
(Pollinator)
1st or Breba
(Summer)
None
Parthenocarpic
Parthenocarpic
Profichi ***
2nd or Main
(Summer/Fall)
Caprification
Caprification
Parthenocarpic
Mammoni
3rd Crop
(Overwinter)
None
None
None
Mamme

 * Depending on the cultivar, main crop may develop even if it is not caprified.
 ** There are about 400-500 cultivated varieties of the common fig (Ficus carica).
*** Only the caprifig profichi crop produces pollen, and this is used to pollinate
    (caprify) the receptive main crop of Smyrna & San Pedro type figs in June.

Longitudinal section through a caprifig profichi syconium in June showing male flowers.

Left: Caprifig with developing mammoni crop of syconia. Right: F. carica cultivar 'Calimyrna' with developing 2nd or main crop of syconia. Both of these syconia form in early summer on new growth. They mature in late summer to early fall. The immature Calimyrna main crop is pollinated (caprified) in June by wasps carrying pollen from the previous profichi crop of caprifigs. Without caprification this main crop will drop from the tree, a trait known as caducous. The mature mammoni syconia will release another generation of female fig wasps who will enter the 3rd or mamme crop of caprifigs in the fall. This crop will overwinter on the tree when all the leaves have fallen.


8. Ficus carica With Persistent vs. Caducous (Early Deciduous) Syconia

According to W.B. Storey (1975), there is a dominant mutant allele (P) for persistent syconia and ovule abortion. This allele is egg lethal so it can only be carried in the sperm. In other words, it cannot be passed on from a persistent female tree. The homozygous genotype PP is not possible. A recessive wild type allele (+) results in caducous syconia and normal ovule development. It can be carried by the egg and sperm. Therefore the only possible genotypes for caprifigs and female trees are P+ and ++. Persistent caprifigs and persistent female trees must be heterozygous (P+). Mature pollinated syconia on heterozygous female trees having the allele for persistence (P) may contain hollow drupelets (cenocarps) as well as normal seed-bearing druplets. Although I don't have a specific reference, I don't see why the persistent allele (P) could not occur in wild populations of F. carica. This allele does not appear advantageous to the female fig, although if wasp-bearing caprifigs are nearby the syconia are capable of producing seeds.

This is a complicated subject when discussing the biology of Ficus carica. In general, unpollinated parthenocarpic cultivars with the persistent gene must be propagated by cuttings because the druplets in their syconia are hollow cenocarps without seeds. These cultivars have been grown and selected for flavorful "figs" and, like many other excellent fruit cultivars, must be propagated asexually in order to obtain clones. Cultivars such as the 'Verte' are valuable because they are absolutely delicious and do not require wasp pollination in order to set fruit. If these parthenocarpic cultivars are pollinated by a nearby caprifig they can produce seed-bearing druplets in addition to hollow druplets (cenocarps). The remains of female F. carica syconia have been discovered in archaeological sites of the Jordon Valley that date back 11,400 years. They are clearly persistent, parthenocarpic syconia containing hollow druplets (cenocarps). When M.E. Kislev concluded they were planted by cuttings and possibly represented the first known domesticated plants, perhaps he assumed that the trait for persistent syconia was unique to seedless fig cultivars. According to Storey (1975), this gene can occur in both female trees and caprifigs. It is passed to female progeny in the sperm of caprifig pollen parents. Female parthenocarpic trees with the persistent gene can produce seeds if they are pollinated by fig wasps. The ancient syconia of the Jordon Valley with hollow cenocarps could have come from unpollinated female trees that grew from seeds.

  See Section On Early Domestication Of Ficus carica In The Jordan Valley  

P = Dominant allele for persistent syconia & ovule abortion (egg lethal). Mutant allele Acc. to Storey (1975)
+ = Recessive allele for caducous syconia & normal ovule development.  Wild Allele Acc. To Storey (1975)

Genetics of Persistent Vs. Caducous Alleles in Ficus carica.

Following table based on Storey, W.B. 1975. "Figs." In: Advances in Fruit Breeding, Purdue Univ. Press, 1975, pp. 568-589. Originally from
Saleeb, W.F. 1965. "Genetics and Cytology of Syconium Persistence in Ficus carica." Ph.D. Dissertation, Univ. of California, Riverside.

Female Fig
Genotype
Eggs
Caprifig
Genotype
Pollen
Progeny
Genotype
++
+
++
+
All ++
P+
+ (P dies)
++
+
All ++
++
+
P+
P and +
1 P+: 1 ++
P+
+ (P dies)
P+
P and +
1 P+: 1++

Cross Between Persistent Female Tree (P+) and Persistent Caprifig (P+):

Alleles in Eggs Of Seed Parent
P is "Egg Lethal" & Cannot Be in Egg
PP and P+ Progeny Not Possible
Alleles In Sperm Of Caprifig Pollen Parent
P
+
-----
-----
-----
+
P+
++

Cross Between Persistent Female Tree (P+) and Caducous Caprifig (++):

Alleles in Eggs Of Seed Parent
P is "Egg Lethal" & Cannot Be in Egg
Heterozygous P+ Progeny Not Possible
Alleles In Sperm Of Caprifig Pollen Parent
+
+
-----
-----
-----
+
++
++

Cross Between Caducous Female Tree (++) and Persistent Caprifig (P+):

Alleles in Eggs Of Seed Parent
Heterozygous P+ Progeny Possible
Because P Allele Carried By Sperm
Alleles In Sperm Of Caprifig Pollen Parent
P
+
+
P+
++
+
P+
++

Above tables based on Storey, W.B. 1975. "Figs." In: Advances in Fruit Breeding, Purdue Univ. Press, 1975, pp. 568-589. Originally from
Saleeb, W.F. 1965. "Genetics and Cytology of Syconium Persistence in Ficus carica." Ph.D. Dissertation, Univ. of California, Riverside.


9. The Ficus pseudocarica - F. palmata Controversy

According to Ira Condit's monograph on fig varieties (1955), the caprifig of this species has a distinctive profichi syconium that is purple-black in color with a long, slender stalk (peduncle). In his classic volume The Fig (1947), Condit describes the syconium as smaller than other varieties of F. carica. In Ficus: The Exotic Species (1969), Condit describes the twigs of F. pseudocarica as velvety pubescent and the twigs of F. carica as glabrous or only slightly puberulent when young. F. pseudocarica is listed as a synonym of F. palmata (Punjab fig) in the Kew List Of Plant Species (2011). It is listed as naturalized in California (under F. palmata) in the Calflora Database and USDA Plant Database. According to the revised Jepson Manual (2011), reports of F. pseudocarica and F. palmata are based on misidentified specimens of F. carica (A.T. Whittemore, 2006, Sida 22: 769-775).

According to Condit (1955), Ficus pseudocarica is native to Eritrea and Abyssinia, while F. palmata is indigenous to Pakistan, northern India and Afghanistan. He states that F. pseudocarica was introduced into Santa Barbara, California in 1902, and like F. palmata, was used for hybridizing with F. carica. In fact, the edible 'Brawley' caprifig cultivar is a hybrid between F. carica var. 'kadota' and a F. pseudocarica caprifig (Storey et al. 1977). Ficus palmata is commonly used in modern floras, with F. pseudocarica listed as a synonym. Alan Whittemore (2006) has studied herbarium collections of F. palmata (F. pseudocarica) from California and has concluded that they are misidentified and should be labeled F. carica. He compared 4 collections of "F. palmata" by H.M. Pollard from Cold Spring Canyon, Santa Barbara Co. during the 1950s with 31 sheets of F. palmata from India, Nepal, Pakistan, Saudi Arabia, Yemen, Eritrea and Ethiopia and 70 sheets of cultivated F. carica worldwide. [Interestingly enough, Pollard's 1950 collections at Rancho Santa Ana Botanic Garden are labeled F. pseudocaria.] Whittemore used 14 characteristics in his analysis of Pollard's sheets, 10 of which matched F. carica better than F. palmata. According to Whittemore, F. palmata (F. pseudocarica) was occasionally grown horticulturally in California, but there is no evidence that it ever escaped from cultivation.

Mallikarjuna Aradhya et al. (2010) studied 194 fig accessions maintained at the USDA National Clonal Germplasm Repository, Davis, California. Their extensive DNA cladogram shows F. pseudocarica on a sister clade with the 'Hacin' cultivar of F. carica, between clades of the popular F. carica cultivars 'Zidi' and 'Roeding.' All of these varieties were derived from the ancestral F. pumila. Under "Materials and Methods," Aradhya et al. cite the single accession of F. pseudocarica as a synonym of F. palmata. Dna cladograms by Nina Rønsted et al. (2005 and 2006) show F. palmata in a clade far away from F. pumila and certainly not derived from F. pumila. In another cladogram by Rønsted et al. (2008), Ficus pumila (Subsection Frutescentiae) is placed close to F. palmata (Subsection Ficus). In the latter cladogram, the sister clade of F. palmata is F. johannis, another closely-related deciduous fig in the Ficus carica-F. palmata complex. F. pumila has been artificially crossed with F. carica, indicating a close genetic relationship. It is unfortunate that F. carica was not included in these phylogenetic trees.

Ficus pseudocarica and F. palmata at test plots of UC Riverside in June 1985.

The leaves of F. palmata are quite distinctive and match illustrations and photos of the tree in its native habitat from Ethiopia to India; however, according to Condit (1969) the leaves can also be deeply lobed. Condit lists Blastophaga psenes as the symbiotic pollinator wasp for F. palmata, the same species found in F. carica. K.J. Joseph (1954) reported B. vaidi for F. palmata in India, but Wiebes and Compton (1990) consider this species of wasp questionable because it is so similar morphologically to B. psenes. The nonpollinator wasps Sycoscapter forsteni and Philotrypesis palmata are also reported for F. palmata in India (S. van Noort and A. van Harten, 2006). Although the obligate mutualism between pollinating fig wasps and their host fig trees has historically been a one-to-one relationship, more than one species of pollinator wasp can be associated with a single host and, conversely, a single pollinator can be associated with more than one host fig species (van Noort and van Harten, 2006; van Noort and Rasplus, 2010).

Ficus pseudocarica is an enigma. In the DNA cladogram of Aradhya et al. (2010), the clade of a specimen identified as F. pseudocarica is embedded within clades of F. carica cultivars and yet it is considered synonymous with F. palmata. It seems reasonable to assume that if F. pseudocarica is synonymous with F. palmata and if F. palmata is a valid species, it should be in a clade separate from F. carica. These discrepencies suggest that perhaps some collections identified as F. pseudocarica in California are varieties of F. carica.

During the past two decades, a number of additional fig collections have been made in southern California by reputable botanists who concluded the species was Ficus palmata rather than F. carica. Eight of these are listed by the Consortium of California Herbaria at Rancho Santa Ana Botanic Garden and University of California, Riverside. DNA evidence strongly suggests that these two species are closely related; however, major herbaria such as Kew and Missouri Botanical Garden recognize them as distinct species. Although my 1986 caprifig collection from Vista, California (RSA381641) has some characteristics matching Condit's description of F. pseudocarica, it is perhaps best treated as a variety of Ficus carica.

In Ficus: The Exotic Species (1969) Condit discusses the difficulty in separating Ficus palmata from F. pseudocarica. In fact, in his Key To Ficus, the two species are not separated. Even the separation between these two species and Ficus carica is only based on the degree of pubescence of young stems. Ficus carica twigs are glabrous or only slightly puberulent, while those of F. pseudocarica and F. palmata are velvety pubescent. Other characteristics, such as leaf shape and size, venation, and the size, shape and color of fruit are so variable that it is difficult to make a positive identification from the key. Under his description of Ficus palmata, Condit cites George King who studied these species in the late 1800s: "I have a strong suspicion that all may be but forms of F. carica Linn." According to the extensive fig website FigWeb (2011), fig biologists Simon van Noort and Jean-Yves Rasplus state that F. palmata and F. carica are probably conspecific. The Principle of Parsimony (Occam's Razor) states that the least complex explanation for an oberservation is probably the best explanation. If F. pseudocarica, F. palmata and F. carica are all taxonomic varieties or subspecies of one species complex, the above discrepencies between DNA analysis and disputed California collections of these species might be resolved!

  Cladogram Comparing DNA Of Ficus carica Varieties (PDF file)  


10. Sex Determination By Genes & Chromosomes in Ficus carica

      G = dominant allele for short-style female flowers
      g = recessive allele for long-style female flowers
      A = dominant allele for production of male flowers
      a = recessive allele for suppression of male flowers
Dominant G & A genes linked on one chromosome.
    Recessive g & a genes on homologous chromosome.
    
Fig Genotypes:
Caprifig: GA/GA & Heterozygous GA/ga.
Female fig: Homozygous ga/ga ONLY.

Storey, W.B. 1975. "Figs." In: Advances in Fruit Breeding. J. Janick & J.N. Moore, Eds. Purdue Univ. Press, 1975.
Storey, W.B. 1955. "Sex Inheritance in Figs." Calif. Fig Institute. Proceedings of the Annual Conference 9: 15-17.

It is interesting to note that Dr. Storey's original discovery that sex determination in Ficus carica is under the control of a single autosomal locus, and that functional males are heterogametic for sex determination was corrobarated by T.L. Parish, H.O. Koelewijn, and P.J. van Dijk in 2004 (Sexual Plant Reproduction 17: 17-22). They studied DNA fragments (Amplified Restriction Length Polymorphisms or AFLPs) in the gynodioecious species Ficus fulva.

Seed Parents
Pollen Parents
Homo Caprifig (GA/GA)
[GA] only
Hetero Caprifig (GA/ga)
[GA] and [ga]
Homo Caprifig (GA/GA)
[GA] only
All GA/GA Male
1/2 GA/GA Male
1/2 GA/ga Male
Hetero Caprifig (GA/ga)
[GA] and [ga]
1/2 GA/GA Male
1/2 GA/ga Male
1/4 GA/GA Male
1/2 GA/ga Male
1/4 ga/ga Female
Female Fig (ga/ga)
[ga] only
All GA/ga Male
1/2 GA/ga Male *
1/2 ga/ga Female *

* = Most likely genotypic combination: Homozygous female tree x heterozygous caprifig.

  Sex Determination & Life Cycle Of Ficus carica  


11. 'Calimyrna' ('Sari Lop') Fig Orchard In San Joaquin Valley

Each June in California's hot San Joaquin Valley, paper bags containing wasp and pollen-bearing caprifigs are stapled to limbs in Calimyrna fig orchards. Only a few wasp-laden caprifig syconia are placed in the bags to prevent overpollination and split Calimyna fruit. Inside the paper bag (right), small black wasps can be seen exititing the caprifigs.

A wasp-pollinated Calimyrna fig containing numerous seed-bearing druplets (minute ripened ovaries). In fact, the excessive pollination and seed production has caused the syconium to split open. The seed-bearing drupelets impart a superior nutty flavor to the fig newton (right).


12. The Actual Ripened Botanical Fruits Of A Fig

The actual botanical fruits of figs are the minute one-seeded drupelets that line the inside of the syconium. The syconium is a structure unique to Ficus. It is a hollow inflorescence lined on the inside by numerous unisexual, apetalous flowers. The ovaries of long-style flowers develop into one-seeded drupelets if they are pollinated.

In short-style female flowers, the wasp inserts her ovipositor down the stylar canal and lays an egg in the ovary of the flower. The subsequent larva feeds on endosperm tissue initiated by the ovipositing pollinator wasp. Since the endosperm in some figs may be initiated parthenogenetically (without pollination and fertilization), possibly by a mechanical or chemical stimulus during oviposition, food tissue for the developing larva functions like a minute gall. According to Saleeb (1965), the parthenogenetic endosperm of Ficus carica is the same as the sporphyte tissue (2n = 26), showing that it did not result from double fertilization. Style length is genetically controlled, and it is important for the tree to have style lengths longer than the wasp's ovipositor in long-style flowers so that seeds can develop in these ovaries. It is also important to have flowers with short styles so that female wasps can lay eggs (oviposit) in the ovaries. "Bogus" fig wasps (parasitoids and inquilines) with extra long ovipositors present a formidable problem to figs. They can readily lay eggs in long-style flowers, and can even penetrate the syconium wall without pollinating the female flowers inside. Some dioecious figs can counter this problem by simply aborting unpollinated syconia, thus ridding itself of seedless syconia. This strategy does not work on monoecious figs with multiple style lengths in the same syconium. Dioecious figs may represent an advanced (further evolved) species.


13. Overwintering Mamme Crop Of A Caprifig


Overwintering mamme crop of syconia.

Left: Leafless (dormant) caprifig photographed in February 2009 showing overwintering mamme crop and spring profichi crop of syconia. Right: A fig wasp larva inside the ovary of a short-style female flower in an overwintering mamme syconium. Since the previous fall mammoni crop of syconia do not produce pollen, the larva fed on parthenogenetic endosperm tissue in the mamme syconium that developed without pollination. The initiation of endosperm tissue after oviposition by the female wasp meets the criterion for gall formation. The larva consumes the galled tissue within the ovary wall. After metamorphosis, the adult male wasp chews a hole through the ovary wall and exits the female flower. He then crawls to another short-style female flower that contains a mature female wasp. He climbs up on the ovary of the flower, bites a fertilization hole in the ovary wall, and inserts his long, slender abdomen into the opening, thus inseminating the female. After being inseminated, the female crawls out of the fertilization hole through the ovary wall initially made by the male. My students and I observed this phenomenum many times during general biology laboratory sessions.

A dozen female Blastophaga psenes crammed into the ostiole of receptive profichi syconium of a caprifig. Photographed 25 March 2009. These winged female wasps came from the overwintering mamme crop on the caprifig tree.


14. Why Can't Female Wasp Lay Her Eggs Inside Syconium Of Edible Fig?

Syconium of edible fig (female tree) lined on the inside with dense mass of long-style female flowers. Ovipositor of wasp is too short to penetrate the ovaries of these flowers, so she is unable to oviposit. Her wings typically break off as she squeezes through the ostiole and bracts. She will eventually die inside this syconium, but during her attempts to oviposit, she will pollinated the long-style female flowers. The ovaries of these flowers will develop into seed-bearing drupelets.


15. Vicarious Selection In Dioecious Figs

A plausible explanation why pollinator wasps don't evolve longer ovipositors so they can oviposit in the ovaries of long-style female flowers. Male and female syconia are virtually indistinguishable in external appearance. Selection takes place in male syconia of caprifig.

In his book "Climbing Mount Improbable (1996), Richard Dawkins devotes Chapter 10 to the fig/fig wasp coevolution and the model for vicarious selection proposed by Grafen and Godfray (Proceedings of the Royal Society, 1991). In vicarious selection of the dioecious fig subgenus Urostigma, morphology (style and ovipositor length), and wasp behavior (purposive loading and unloading of pollen) is taking place in wasps who enter and leave male syconia containing short-style female flowers on male trees. This selection is crucial for the perpetuation of fig trees when wasps enter female syconia on female trees (which superficially resemble male syconia). Female syconia produce seeds (the vital genetic link for fig trees) and are a genetic graveyard for wasps because they cannot oviposit in the long-style female flowers. The female wasps die in these syconia. For wasps in female syconia, mutations for a longer ovipositor that could reach the ovary of long-style flowers would not be passed on. For wasps in male syconia, there is no selective advantage for longer ovipositors because they are perfectly adapted for laying eggs in the ovaries of short-style flowers. Vicarious selection does not explain the evolution of ovipositor length in all figs, particularly the numerouas monoecious species. The fig/fig wasp scenario is much more complicated, with many variations in the life cycles depending on the different subgenera. Unfortunately, it is beyond the scope of this discussion.

   See Key To The Subgroups Of Dioecious Figs   

In about half of the fig species (referred to as monoecious), male flowers and the long and short-style female flowers occur in the same bisexual syconium; but in all other fig species (referred to as dioecious), the seed-producing, long-style female flowers only occur in unisexual syconia on female trees, while pollen-bearing male flowers and wasp-bearing, short-style female flowers occur in the same syconia on male trees. This latter arrangement is typical of the common fig. In fact, early fig growers in California's San Joaquin Valley were puzzled why their imported Smyrna figs would not set fruit. The trees didn't have their symbiotic wasp from Asia Minor and dropped their their crops of unpollinated syconia.


16. Parthenocarpic Varieties Of Ficus carica

There are many cultivated "parthenocarpic" varieties of the common fig in which the syconia develop on female trees without wasp pollination. The ripe syconia are fleshy and edible; however, the numerous ovaries (drupelets) inside are hollow and seedless. Examples of these varieties include 'Brown Turkey,' 'Mission' and 'Kadota.' The remains of parthenocarpic fig syconia in ancient settlements of the Jordon Valley indicate the people recognized natural parthenocarpic trees and propagated them by cuttings more than 11,000 years ago. According to fig connoisseurs, pollination produces a more delicious fig with a superior nutty flavor due to the seeds. In fact, the best fig newtons come from wasp pollinated 'Calimyrna' fig orchards in Fresno and Madera Counties. Most of the trees are female, but growers also maintain small groves of wasp and pollen-bearing male trees called caprifigs. The prefix capri refers to goat, and these inedible figs were fed to goats in the Old Word.

Fig Cultivation Predates Cereal Domestication

Kislev, M.E., Hartmann, A. and O. Bar-Yosef. 2006. "Early Domesticated
Fig in the Jordan Valley." Science 312 (5778): 1372-1374. 2 June 2006

The remains of parthenocarpic fig syconia (edible figs) have been discovered in archeological sites of the Jordon Valley that date back to 11,400 years bp. The carbonized syconia are clearly parthenocarpic because the drupelets are without embryos or seeds. Wild populations of Ficus carica are gynodioecious with male trees (caprifigs) and female trees. Edible figs are produced on female trees only if they are pollinated by fig wasps (Blastophaga psenes) from the syconia of male trees. The male syconia contain wasps and pollen, and are generally not eaten. They were named "caprifigs" because they were commonly fed to goats. If pollinated, seeds develop inside the druplets within syconia on female trees. Without pollination, the immature figs are shed by the female trees. According to W.B. Storey (1975), parthenocarpy is produced by a single domant mutant gene. Female trees expressing this gene retain their developing figs to maturity, even though they are not pollinated and contain no seeds. Parthenocarpic trees must be propagated by cuttings because they do not produce seeds. They produce sweet fig fruits (syconia) without the need for male trees that carry symbiotic fig wasps within their syconia. This is very advantageous to farmers in regions where the wild caprifigs and natural pollinator wasps do not occur. The presence of parthenocarpic figs in ancient settlements indicates that people recognized these rare parthenocarpic trees and propagated them by planting branches. Evidence of such activity may mark one of the earliest forms of agriculture. Fig trees could have been the first domesticated plant of the Neolithic Revolution, which preceded cereal domestication by about 1,000 years.

Fig Cultivation May Not Predate Cereal Domestication

Lev-Yadum, S., Ne´eman, G., Abbo, S., and M.A. Flaishman. 2006. "Comment on Early
Domesticated Fig in the Jordan Valley." Science 314: 1683a. 15 December 2006

Parthenocarpic trees of Ficus carica produce 1 or 2 annual crops of seedless syconia (see Table of Fig Crops). They are all capable of producing seeds if they are pollinated by caprifigs containing fig wasps and pollen. These parthenocarpic syconia could have come from wild trees that grew from seeds. "Because all parthenocarpic fig types can produce seeds, the finds described in (1) cannot serve as an unambiguous sign of cultivation and lend no support to the notion that horticulture predated grain crops in the Near East."

Left: 'Brown Turkey', a parthenocarpic variety (cultivar) of the common fig (Ficus carica). Right: Another parthenocarpic variety of F. carica similar to 'Verte'. It produces a heavy 2nd (main crop) late in the fall (October-November). The syconia have a green outer skin and strawberry interior. This is the most delicious, sweet fig that I have ever eaten.

Seed-bearing endocarps of Ficus carica variety 'Verte' at the bottom of a dish of water. Although this cultivar is parthenocarpic, it has been pollinated by fig wasps from a nearby caprifig. Endocarps with mature, viable seeds typically sink in water. These are the actual fruits of a fig. They are the sclerified inner layer of tiny, ovule-bearing ovaries after the thin, fleshy, outer pericarp layer has been removed. Hollow (seedless) drupelets produced without pollination and fertilization are called cenocarps. If the endocarps contain wasp larvae they are called psenocarps.

Dried fig varieties from Bates Nut Farm, San Diego County. Left: Black Mission. Right: Calimyrna

  See More Parthenocarpic Varieties Of The Common Fig (Ficus carica)   


17. Dangers Facing The Emerging Female Fig Wasps

The emerging female fig wasp faces many dangers after she leaves the safety of her protective syconium. One of these dangers during wasp exodus from summer profichi and fall mammoni crops of syconia on Ficus carica are predators, including opportunistic spiders. The following image shows a minute orb weaver called the trashline spider (Cyclosa turbinata) that has built its web near a mammoni syconium of Ficus pseudocarica = F. carica. On September 14, many wasps leaving the syconium fluttered into the web and were quicky caught by the tiny spider. This minute orb weaver spider (family Araneidae) is only about 5 mm long. It is called the trashline spider because it stores it victims, each rolled in cases of silk, in a vertical row in the center of the web.


18. Which Figs Grew In The Ancient Holy Land?

Kalamata string figs. In ancient times people carried strings of dried figs such as these on long arduous journeys across the desert. The figs provided them with a nutritious high protein, high carbohydrate food source in a region where food was scarce.

An excellent article entitled "The History of the Fig in the Holy Land from Ancient Times to the Present" was written by Asaph Goor in Economic Botany 19: 124-135 (1965). The fig species discussed by Goor is the common edible fig (Ficus carica). This tree was cultivated for its fruit more than 11,000 years ago and is native to the region between the Mediterranean and Black Seas, sometimes referred to as the ancient region of Caria in Asia Minor. It is a dioecious species with separate male and female trees, and a symbiotic pollinator wasp (Blastophaga psenes) that is propagated inside the fruits (syconia) of male trees called caprifigs. It grows wild over a large area, including southern Europe and the Middle East. Goor (1965) stated that Ficus carica grew wild in the Holy Land thousands of years ago; however, this doesn't necessarily mean that it was truly native (indigenous) to the Holy Land. It may have been introduced by people to this region, either by seeds or cuttings.

According to M.E. Krislev, A. Hartmann, and O. Bar-Yosef, "Early Domesticated Fig in the Jordan Valley," Science 312: 1273-1275 (June 2006), the remains of parthenocarpic fig syconia (edible figs) have been discovered in archeological sites of the Jordon Valley that date back to 11,400 years bp. The carbonized syconia are clearly parthenocarpic because the drupelets are without embryos or seeds. Edible figs are produced on female trees only if they are pollinated by fig wasps (Blastophaga psenes) from the syconia of male trees. The male syconia contain wasps and pollen, and are generally not eaten. They were named "caprifigs" because they were commonly fed to goats. If pollinated, seeds develop inside the druplets within syconia on female trees. Without pollination, the immature figs are shed by the female trees. According to W.B. Storey (1975), parthenocarpy is produced by a single domant mutant gene. Female trees expressing this gene retain their developing figs to maturity, even though they are not pollinated and contain no seeds. Parthenocarpic trees must be propagated by cuttings because they do not produce seeds. They produce sweet fig fruits without the need for male trees that carry symbiotic fig wasps within their syconia. This is very advantageous to farmers in regions where the wild caprifigs and natural pollinator wasps do not occur. The presence of parthenocarpic figs in ancient settlements indicates that people recognized these rare parthenocarpic trees and propagated them by planting branches. Evidence of such activity may mark one of the earliest forms of agriculture. Fig trees could have been the first domesticated plant of the Neolithic Revolution, which preceded cereal domestication by about 1,000 years.

Ficus carica and its symbiotic wasp have even been introduced into California, including male and female trees that grow wild in San Diego County. The symbiotic wasps live in a caprifigs that produce three crops of inedible figs (syconia) each year, including a wasp-bearing, overwintering mamme crop that remains on the bare branches when the tree is devoid of leaves. There are several varieties of male caprifigs and hundreds of varieties of female Ficus carica trees, some of which develop delicious, seedless, parthenocarpic fruits that do not require pollination. There are also varieties in which the female trees will shed their entire crop if they are not pollinated by the symbiotic fig wasp. These varieties have been selected by people over countless centuries. The trees are readily propagated by cuttings and were transported and cultivated by people thousands of years ago. Apparently many ancient civilizations were aware of the fact that Ficus carica required pollination in order to produce edible, seed-bearing fruits, a process called caprification. In 350 B.C., Aristotle described fig wasps that came out of caprifigs and penetrated the unripe female fig fruits, thus fertilizing them. Theophrastus (372?-287? B.C.) discussed caprification in detail, and Pliny (23-79 A.D.) devoted an entire chapter to the practice of caprification in Italy. The subject of fig pollination and "gallflies" in ancient Babylonia is also mentioned by Herodotus (Book I, 485?-425? B.C.). Early horticulturists were undoubtedly aware that the seeds impart a superior, nutty flavor to the fruit, and in some varieties the fruit will not set if it is not pollinated by fig wasps. The fig referred to in ancient Babylonia was probably Ficus carica, but another species called the sycomore fig (Ficus sycomorus) was also used for food in the eastern Mediterranean region. According to Goor (1965): "The sycomore fruit is much inferior and cheaper... It is eaten by the poorer classes and by shepherds in plains where it grows alone." In addition it does not survive cold winters like Ficus carica, and Ficus carica has a much wider range, particularly in colder regions of Iraq and northward.

An excellent article about ancient fig cultivation was written by J. Galil entitled "An Ancient Technique for Ripening Sycomore Fruit in East-Mediterranean Countries" (Economic Botany 22: 178-190, 1978). When the term "fig gashing" in the Near and Middle East is mentioned in various articles and books (including the Bible), it most likely refers to the sycomore fig (Ficus sycomorus). Although it is native to eastern Central Africa, the sycomore fig was carried north to the Middle East by 3000 BC. Without its native symbiotic pollinator wasp (Ceratosolen arabicus) the trees did not set fruit. Early farmers in this region learned how to induce parthenocarpy by gashing the syconia with a knife. Within 3-4 days the hard, green syconia enlarge and become sweet and fleshy. Gashed sycomore figs have been found in ancient tombs and are depicted in ancient bas-reliefs. Some biblical scholars think the phrase "gatherer of sycomore fruit" (Amos 7:14) actually means "piercer of sycomore fruit." The gashed figs produce ethylene gas which hastens the ripening process. Ethylene gas is also used on green bananas before they reach your supermarket.

There is also a nonpollinator wasp Sycophaga sycomori that lays eggs inside the female flowers of Ficus sycomorus. Symbiotic pollinator wasps of figs (including Ceratosolen arabicus) typically only lay eggs in short-style flowers within the syconium. Their ovipositors are too short to lay eggs in long-style flowers. Consequently, the long-style flowers do not contain wasp larvae and develop seeds instead. This is vital to the tree. The Sycophaga wasp has a longer ovipositor and lays egges in short- and long-style flowers. Therfore, sycomore fig syconia do not bear seeds, only Sycophaga wasps. Apparently the act of oviposition by Sycophaga wasps causes the seedless syconia to enlarge and ripen like gashed figs except they are full of wasps! The trees do not benefit from this relationship because no seeds are produced. Apparently there is also a parthenocarpic variety that will develop edible seedless syconia on its own without Sycophaga wasps. The latter figs do not require gashing. Again, these parthnocarpic (seedless) fruits are not advantageous to the fig tree. This is indeed a complicated subject.

According to J. Galil (1967) there are to ways that sycomore figs develop seedless parthenocarpic fruit without pollination in Israel. Apparently the nonpollinator wasp Sycophaga sycomori has now migrated to this region from Central Africa.

1. Stimulative Parthenocarpy: The nonpollinator wasp Sycophaga sycomori enters the immature syconia causing them to enlarge and develop (ripen) into seedless fruit full of wasps.

2. Vegetative Parthenocarpy: This is apparently a variety of sycomore fig that bears ripe seedless fruit on its own without wasps. This is similar to varieties of the common fig (Ficus carica) that bear edible seedless fruit without pollination.

  See Ancient Figs Of The Holy Land  


19. Fossil Fig Syconia In Wyoming & Montana?

Fossilized (petrified) fig syconia are very difficult to find because they decay rapidy. In 1881, a remarkable discovery was made in the Lance Formation of Converse County, Wyoming by J.B. Hatcher. The syconia had the perfect shape of a modern fig, with a narrowed neck region (peduncle) and a globose body. In fact, they were originally thought to be bulbs of a monocotyledonous plant. Most of the peduncles were broken, but an entrance to the interior (ostiole) at the opposite end was visible on some of the syconia. According to F.H. Knowlton (Bulletin of the Torrey Botanical Club Vol. 38) who described this species in 1911, the interior cavity was filled with course sandstone mixed with extraneous matter, such as bits of vegetation and fragments of shells. According to Knowlton (1911): "In no case was the cavity found to contain seeds, which seems rather remarkable considering the fine state of preservation of the fruit as a whole. It seems probable that when the neck was broken the larger, globose end, being heavier, floated downward and the fruits were filled and covered up in this upright position in which they are found."

The fossil fig was named Ficus ceratops by F.H. Knowlton (1911). The type locality where the original specimen was collected is also called "Ceratops Beds" because of the abundant fossils of late Cretaceous horned (ceratopsid) dinosaurs. These dinosaurs include the well-known Triceratops made popular in the movie Jurassic Park. It weighed up to 12 tons, larger than an elephant. It was armed with huge horns over one meter long and an enormous parrot-like beak with an incredibly strong bite force. Undoubtedy it needed this armor to defend itself against T-Rex that also roamed this region. Incidentally, Knowlton also named the Triassic conifer Araucarioxylon arizonicum in 1889, the state fossil of Arizona.

Petrified "fig syconia" from the badlands of eastern Montana (Dawson County). They were originally thought to be from an extinct species of fig (Ficus ceratops) dating back to the late Cretaceous Period (70 million years ago). Tracks and fossils of T-Rex have also been found in this region of Montana. Right: One of these so-called "fig syconia" is 70 million years old! The other two are dried Mission and Calimyrna figs purchased at a nearby grocery store. Note: The fine longitudinal striations are not characteristic of fig syconia. In fact, these "fig syconia" might actually be endocarps of an extinct palm. See following explanation: "Ficus ceratops May Not Be A Fig."

A. Fibrous mesocarp from the fruit of Normanbya normanbyi, a tropical palm native to rain forests of Australia. B. Permineralized fruit of Spinifructus ceratops from the badlands of eastern Montana. The similar fibrous mesocarp is strong evidence that this fossil fruit is not a fig syconium.
Ficus ceratops May Not Be A Fig!

Astrocaryum huicungo
Like so many other aspects of fig biology, even the identification of fossil syconia is controversial. Several authors have suggested that some of the fig-like fossils from the Hell Creek Formation might belong to a different plant family. According to Alan Graham (1962), the fossil syconia differ from fig fruits is several respects: "The 2-layered pericarp wall, coarse striations at the base of the globose portion of the specimens, and the collar at the proximal end of the stalk are not characteristic of Ficus fruits. These morphological features are evident, however, on fruits of Guarea (Melicaeae)." Elisabeth McIver (2002) has studied these "figs" associated with fossils of Tyrannosaurus rex from southwestern Saskatchewan, Canada. She has transferred them to the new taxon Spinifructus antiquus of an unknown family and order. She suggested that they may be from an arecoid palm with pear-shaped fruits similar to the genera Astrocaryum, Asterogyne or Barcella.

The above image shows the large seed-bearing fruits and endocarps of the starnut palm (Astrocaryum huicungo) from the Rio Napo, a tributary of the Amazon River in Ecuador. This palm is named from the starlike design surrounding the three germination pores an the wide end of endocarps. They have the fibrous longitudinal striations and general shape of Spinifructus. The apex of endocarps have three distinct germination pores that are not visible on the fossil Spinifructus antiquus (syn. Ficus ceratops). These palm fruits are produced in dense clusters.

Phytelephas aequatorialis

Astrocaryum alatum
Palm Fruits With Pointed Projections & Spines
Elisabeth McIver (2002) suggested that the fruits of Spinifructus antiquus might be similar to palms of the genus Astrocaryum. In his on-line article entitled "Dangerous Palms," Geoff Stein has a image of the spine-covered fruits of Astrocaryum alatum (upper right).

  See "Dangerous Palms" By Geoff Stein  

The preconceived stereotype of a fig is something resembling a pear-shaped edible fig (Ficus carica) or dried figs at the supermarket. This is the mistake I made when I first saw these permineralized fruits. Actually, most of the species of wild tropical figs that I have seen have smaller globose syconia. In addition, fig syconia have very little woody tissue and rot away quickly. Fresh edible figs have a very short shelf life and are commonly dried. Palm fruits occur in large, dense clusters and this would explain the occurence of numerous Spinifructus in one small chunk of ground. In addition, fruits of palms such as Astrocaryum are very fibrous with hard, woody endocarps that would permineralize well (i.e. the contents of lignified cells become replaced by minerals and the fruit literally turns into stone). The presence of spines on the outer pericarp rules out figs. It is interesting that the original description by J.W. Dawson (1875) mentions the spiny outer wall.

The first published name for this fossil "fig" was Aesculus antiquus because the original author J.W. Dawson thought it resembled an ancient species of Aesculus (horsechesnut or buckeye) in 1875. See the horsechestnut fruit (left) photographed in Montana. Apparently most of the fossils don't have the spiny fruit wall. With an outer spiny pericarp, this fossil simply cannot be a fig syconium (Ficus). Knowlton did not cite Dawson in his 1911 paper where he describes Ficus ceratops. He was apparently unaware of the spiny outer wall on this fruit. Since Dawson's name predates Knowlton's Ficus ceratops, Dawson becomes the parenthetical author and Elizabeth McIver becomes the new author: Spinifructus antiquus (Dawson) McIver.

Like Knowlton's logs of Petrified Forest National Park (Araucarioxylon arizonicum) that were renamed Pullisilvaxylon arizonicum by R. A. Savidge in 2007, Knowlton's infamous Ficus ceratops has also been renamed by E. McIver in 2002.

  A Taxonomic Problem With Araucarioxylon arizonicum  


A 60 million-year-old fig leaf embedded in hard-rock limestone from the Fort Union Formation near Glendive, Montana. This fossil-rich strata is from the Paleocene Epoch that immediately followed the mass extinction event of dinosaurs at the end of the Cretaceous Period, known as the K-T boundary (Cretaceous-Tertiary boundary). The term Paleocene ("early-recent") refers to a time period when dinosaurs were replaced by smaller mammals, long before modern mammalian orders emerged. The best explanation (scientific theoery) for the demise of non-avian dinosaurs is an enormous 10 km (6 mile) diameter asteroid that collided with the earth causing a global dust cloud that blotted out the sun for many months. Estimates as high as 85 percent of all species disappeared from the face of the earth at this time. This catastrophic event forever changed the direction of the evolution of life on earth.

The K-T boundary is clearly visible in Makoshika Stae Park near Glendive, Montana. It is a dark, narrow band of sediments and carbonized plant material (coal) that separates the Cretaceous and Tertiary periods about 65 million years ago. The tan strata above the K-T band is called the Fort Union Formation. It is younger than 65 million years and does not contain dinosaur fossils. Below the K-T band is the older brownish-gray Hell Creek Formation that is rich in dinosaur fossils, including Tyrannosaurus rex, Triceratops, the amazing duck-billed Hadrosaurus, and the so-called petrified "figs" (Spinifructus antiquuas).

In 1980, a team of researchers consisting of Nobel prize-winning physicist Luis Alvarez, his son, geologist Walter Alvarez, and chemists Frank Asaro and Helen Michels discovered that sedimentary layers found all over the world at the K-T boundary contain a concentration of iridium many times greater than normal. Iridium is a rare earth element that is abundant in most asteroids and comets. It is the second densest element after osmium and the most corrosion-resistant metal. The Alvarez team suggested that an asteroid struck the earth at the time of the K-T boundary.

Above the 65 million year old K-T boundary is the Fort Union Formation & below is the Hell Creek Formation.

Fossil fig leaves have also been reported from the Madro-Tertiary Geoflora in California by Daniel Axelrod (1958). This habitat consisted of semiarid live oak-conifer woodland, chaparral and grassland. Ira Condit (The Fig, 1947) received the following letter from famous paleobotanist Ralph Chaney in 1943: "I have seen a leaf of the carica type from the Miocene of southern California and have no doubt that its relationship to F. carica is extremely close."


20. Complete Index Of On-Line Fig Articles On Wayne's Word

  1. A Petrified Fig Syconium From The Cretaceous Period
  2. Bogus Nonpollinator Fig Wasps With Long Ovipositors
  3. Calimyrna Fig & Its Amazing Pollinator Wasp
  4. Caprifig Fig Overwintering Mamme Crop
  5. Cauliflory In Tropical Species Of Figs (Ficus)
  6. Coevolution Of Fig & Fig Wasp: Vicarious Selection
  7. Evolution Of Dioecious Fig Species
  8. Ficus dammaropsis: A Remarkable Fig From New Guinea
  9. Fig Pith Sculpture: Microscopic Carvings From The Azores
  10. Figs Of The Holy Land (Their Role In World Religions)
  11. Gall Controversy: Do Fig Wasps Really Induce Gall Formation?     
  12. Hybrid Between Common Edible Fig & Creeping Fig
  13. Multiple Fruits Of The Mulberry Family (Moraceae)
  14. Pollination Patterns In Dioecious Figs
  15. Sex Determination & Life Cycle Of Common Fig (Ficus carica)
  16. Sexuality In Figs--Plant Sexuality & Political Correctness
  17. Strangler Figs & Banyans: Truly Remarkable Trees
  18. Summary Of Common Fig (Ficus carica) Life Cycle
  19. The Amazing Fig/Fig Wasp Relationship
  20. The Creeping Fig (Ficus pumila)--Source Of Grass Jelly
  21. Vicarious Selection In Figs (Richard Dawkin's Model)
  22. Wild Figs (Higueras) In Baja California & Gulf Islands
  23. Reference Articles Cited In The Above On-Line Pages

21. Fig References


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