Reproductive coevolution in Ficus

The genus Ficus is composed of 800 species of vines, shrubs, and trees, defined by their syconiums, the fruit-like vessels that either hold female flowers or pollen on the inside. In addition to being cultivated by humans for thousands of years, Ficus is also known for their reproductive mutualism with the fig wasp.[1]

A common fig exposing its many tiny matured, seed-bearing gynoecia. These are pollinated by the fig wasp, Blastophaga psenes. In the cultivated fig, there are also asexual mutants.

Fig trees either produce hermaphrodite fruit known as caprifigs, or female figs; only the female figs are palatable to humans. In exchange for a safe place for their eggs and larvae, fig wasps help pollinate the ficus by crawling inside the tiny hole in the apex of the fig, called the ostiole, without knowing whether they crawled into a caprifig or a fig. If the female wasp crawls into the caprifig, she can successfully lay her eggs and die. The males hatch first, mate with the females, dig tunnels out of the caprifig, and die. The females, now covered in fig pollen from the caprifig, fly out to begin the cycle again. If the female wasp crawls into a female fig, she will not be able to successfully lay her eggs despite pollinating the fig with pollen from the caprifig she hatched in. The fig will absorb her body and her eggs as the fruit develops.[2]

History

Aristotle noted in Historia animalium that wild figs contain psenes that begin as grubs, but whose skin splits allowing the psen to fly out. The psen flies into a cultivated fig, and stops it from falling. He noted further that Greek farmers planted wild figs next to cultivated figs, and tied wild fig fruits on to the cultivated trees.[3]

Mechanisms and outcomes

Overall, the coevolution of Ficus and wasps can be explained through the specificity of Ficus as a host and the tendency of the wasp species to frequent hosts different to that of their original Ficus plant, thus increasing the likelihood of hybrids and eventually new species.

Ficus domination in mutualism

Ficus typically control the reproductive mutualism with fig wasps[4] by being highly selective in their choice of pollinator. Contributing to the evolution of Ficus, pollinator specificity in Ficus is a pre-zygotic mechanism of reproductive isolation among plant species in diverse angiosperm lineages with varying degrees of sympatry and of gene flow in hybrid zones. This is proven by the high host specificity and low pollinator sharing ratios found in fig pollinators, especially in the genera Ceratosolen and Kradibia. Morphological examples of such specificity includes the diameters of ostioles compared to the head widths of the respective wasp species. While the fig species F. wassa have a diameter of 1.0-1.5 mm, its pollinator K. wassae had an average head width of 0.58 mm.[5]

Pollinator-sharing

Pollinator-sharing affects plant species integrity, the delimitation of Ficus species, and the importance of host-switching in shaping the evolutionary history of the mutualism. As indicated by host-pollinator co-phylogenies from neotropical monoecious figs, pollinator-sharing could lead to new host species and host-switching. This could essentially lead to interspecific hybrids in both wasps and figs.[5] A rare possibility is the evolution of cheating in conjunction with a pollinator host shift. In other words, host-sharing species will not even be sister species and may compete for resources. The origin of cheating within a mutualistic lineage has also been shown in yucca moths.[6]

Cospeciation

Despite some significant differences in the fig and pollinator phylogenies, analyses indicate that cospeciation has occurred in the history of the Ficus-wasp mutualism. Contrary to popular belief, the phylogenic conflicts found among figs and wasps are not due to chance differences in the nucleotide substitution patterns in pollinator mtDNA and fig nrDNA. Furthermore, the potential for lineage sorting, a form of genetic drift, in pollinator mtDNA should be low due to inbreeding and small effective population size. Thus, hybridization does not appear to have played a major role in the evolution of fig and pollinator lineages, based on a maximum likelihood test.[6]

References

1. Suleman, Nazia; Sait, Steve; Compton, Stephen G. (2015). "Female figs as traps: Their impact on the dynamics of an experimental fig tree-pollinator-parasitoid community" (PDF). Acta Oecologica. 62: 1–9. Bibcode:2015AcO....62....1S. doi:10.1016/j.actao.2014.11.001.
2. "Fig." Columbia Electronic Encyclopedia, 6th ed.
3. Aristotle. Historia animalium. p. 557b25.
4. Ma, Wen J.; Peng, Yan Q.; Yang, Da-R.; Guan, Jun M. (2009). "Coevolution of reproductive characteristics in three dioecious fig species and their pollinator wasps". Symbiosis. 49 (2): 87–94. doi:10.1007/s13199-009-0018-x.
5. Moe, Annika M. (2011). From pattern to process: Ecology and evolution of host specificity in the fig-pollinator mutualism (PhD Thesis). hdl:11299/117438. OCLC 759912423.
6. Wieblin, George Daniel (1991). Phylogeny and ecology of dioecious fig pollination (PhD Thesis). Ann Arbor: Harvard University. ISBN 978-0-599-51772-1.