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Obligate mutualism within a host drives the extreme specialization of a fig wasp genome.

ABSTRACT: BACKGROUND: Fig pollinating wasps form obligate symbioses with their fig hosts. This mutualism arose approximately 75 million years ago. Unlike many other intimate symbioses, which involve vertical transmission of symbionts to host offspring, female fig wasps fly great distances to transfer horizontally between hosts. In contrast, male wasps are wingless and cannot disperse. Symbionts that keep intimate contact with their hosts often show genome reduction, but it is not clear if the wide dispersal of female fig wasps will counteract this general tendency. We sequenced the genome of the fig wasp Ceratosolen solmsi to address this question. RESULTS: The genome size of the fig wasp C. solmsi is typical of insects, but has undergone dramatic reductions of gene families involved in environmental sensing and detoxification. The streamlined chemosensory ability reflects the overwhelming importance of females finding trees of their only host species, Ficus hispida, during their fleeting adult lives. Despite long-distance dispersal, little need exists for detoxification or environmental protection because fig wasps spend nearly all of their lives inside a largely benign host. Analyses of transcriptomes in females and males at four key life stages reveal that the extreme anatomical sexual dimorphism of fig wasps may result from a strong bias in sex-differential gene expression. CONCLUSIONS: Our comparison of the C. solmsi genome with other insects provides new insights into the evolution of obligate mutualism. The draft genome of the fig wasp, and transcriptomic comparisons between both sexes at four different life stages, provide insights into the molecular basis for the extreme anatomical sexual dimorphism of this species.

SUBMITTER: Xiao JH

PROVIDER: S-EPMC4053974 | biostudies-literature | 2013

REPOSITORIES: biostudies-literature

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Obligate mutualism within a host drives the extreme specialization of a fig wasp genome.

Xiao Jin-Hua JH Yue Zhen Z Jia Ling-Yi LY Yang Xin-Hua XH Niu Li-Hua LH Wang Zhuo Z Zhang Peng P Sun Bao-Fa BF He Shun-Min SM Li Zi Z Xiong Tuan-Lin TL Xin Wen W Gu Hai-Feng HF Wang Bo B Werren John H JH Murphy Robert W RW Wheeler David D Niu Li-Ming LM Ma Guang-Chang GC Tang Ting T Bian Sheng-Nan SN Wang Ning-Xin NX Yang Chun-Yan CY Wang Nan N Fu Yue-Guan YG Li Wen-Zhu WZ Yi Soojin V SV Yang Xing-Yu XY Zhou Qing Q Lu Chang-Xin CX Xu Chun-Yan CY He Li-Juan LJ Yu Li-Li LL Chen Ming M Zheng Yuan Y Wang Shao-Wei SW Zhao Shuang S Li Yan-Hong YH Yu Yang-Yang YY Qian Xiao-Ju XJ Cai Yue Y Bian Lian-Le LL Zhang Shu S Wang Jun-Yi JY Yin Ye Y Xiao Hui H Wang Guan-Hong GH Yu Hui H Wu Wen-Shan WS Cook James M JM Wang Jun J Huang Da-Wei DW

Genome biology 20131220 12

<h4>Background</h4>Fig pollinating wasps form obligate symbioses with their fig hosts. This mutualism arose approximately 75 million years ago. Unlike many other intimate symbioses, which involve vertical transmission of symbionts to host offspring, female fig wasps fly great distances to transfer horizontally between hosts. In contrast, male wasps are wingless and cannot disperse. Symbionts that keep intimate contact with their hosts often show genome reduction, but it is not clear if the wide ...[more]

PMID: 24359812

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Project description:Fig trees are pollinated by fig wasps, which also oviposit in female flowers. The wasp larvae gall and eat developing seeds. Although fig trees benefit from allowing wasps to oviposit, because the wasp offspring disperse pollen, figs must prevent wasps from ovipositing in all flowers, or seed production would cease, and the mutualism would go extinct. In Ficus racemosa, we find that syconia ('figs') that have few foundresses (ovipositing wasps) are underexploited in the summer (few seeds, few galls, many empty ovules) and are overexploited in the winter (few seeds, many galls, few empty ovules). Conversely, syconia with many foundresses produce intermediate numbers of galls and seeds, regardless of season. We use experiments to explain these patterns, and thus, to explain how this mutualism is maintained. In the hot summer, wasps suffer short lifespans and therefore fail to oviposit in many flowers. In contrast, cooler temperatures in the winter permit longer wasp lifespans, which in turn allows most flowers to be exploited by the wasps. However, even in winter, only in syconia that happen to have few foundresses are most flowers turned into galls. In syconia with higher numbers of foundresses, interference competition reduces foundress lifespans, which reduces the proportion of flowers that are galled. We further show that syconia encourage the entry of multiple foundresses by delaying ostiole closure. Taken together, these factors allow fig trees to reduce galling in the wasp-benign winter and boost galling (and pollination) in the wasp-stressing summer. Interference competition has been shown to reduce virulence in pathogenic bacteria. Our results show that interference also maintains cooperation in a classic, cooperative symbiosis, thus linking theories of virulence and mutualism. More generally, our results reveal how frequency-dependent population regulation can occur in the fig-wasp mutualism, and how a host species can 'set the rules of the game' to ensure mutualistic behavior in its symbionts.

Project description:BackgroundAlternative mating tactics are widespread in animals and associated with extreme morphological polymorphism in some insects. Some fig wasps have both highly modified wingless males and dispersing winged males. Wingless males mate inside figs before females disperse, while winged males mate elsewhere after dispersal. Hamilton proposed a model for this system with morphs determined by alternative alleles. This has an equilibrium where the proportion of winged males equals the proportion of females dispersing unmated; i.e. the proportion of matings that they obtain. Previously, we have shown qualitative support for this prediction across nine wing-dimorphic fig wasp species. Here I test the quantitative prediction in the fig wasp Pseudidarnes minerva. In addition, some fig wasp species that lack winged males, but have two wingless morphs, show a conditional strategy with morph determination influenced by the number of wasps developing in a patch. I also test for this alternative pattern in the wing-dimorphic P. minerva.ResultsI sampled 114 figs that contained a mean of 2.1 P. minerva wasps from 44 trees across four sites in Sydney, Australia. At the whole population level, the proportion of winged males (0.84 or 0.79 corrected for sampling bias) did not differ significantly from the proportion of unmated females (0.84), providing strong quantitative support for the prediction of Hamilton's model. In addition, there was no evidence for other factors, such as local mate competition or fighting between wingless males, that could violate simplifying assumptions of the model. Meanwhile, the proportion of winged males was not correlated with the number of wasps per fig, providing no evidence for a conditional strategy.ConclusionThe morph ratio in P. minerva is consistent with Hamilton's simple Mendelian strategy model, where morph ratios are set by average mating opportunities at the population level. This contrasts with some fig wasps from another subfamily that show conditional morph determination, allowing finer scale adaptation to fig-level mating opportunities. However, these conditional cases do not involve wing polymorphism. Male polymorphism is common and variable in fig wasps and has evolved independently in multiple lineages with apparently different underlying mechanisms.

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Obligate mutualism within a host drives the extreme specialization of a fig wasp genome.

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Obligate mutualism within a host drives the extreme specialization of a fig wasp genome.

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