Adaptation of Fig Wasps (Agaodinae) to Their Host Revealed by Large-Scale Transcriptomic Data

Figs and fig wasps are highly species-specific and comprise a model system for studying co-evolution and co-speciation. The evolutionary relationships and molecular adaptations of fig wasps to their fig hosts are poorly understood, and this is in part due to limited sequence data. Here, we present large-scale transcriptomic datasets of 25 fig wasp species with the aim of uncovering the genetic basis for host specificity. Our phylogenetic results support the monophyly of all genera associated with dioecious figs, and two genera associated with monoecious figs, Eupristina and Platyscapa, were revealed to be close relatives. We identified gene loss and gain, potentially rapidly evolving genes, and genes under positive selection. Potentially functional changes were documented and we hypothesize as to how these may determine host specificity. Overall, our study provides new insights into the evolutionary diversification of fig wasps and contributes to our understanding of adaptation in this group.

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Genome-Wide Analysis of Gene Families of Pattern Recognition Receptors in Fig Wasps (Hymenoptera, Chalcidoidea)

Genes ◽

10.3390/genes12121952 ◽

2021 ◽

Vol 12 (12) ◽

pp. 1952

Author(s):

Hong-Xia Hou ◽

Da-Wei Huang ◽

Zhao-Zhe Xin ◽

Jin-Hua Xiao

Keyword(s):

Pattern Recognition ◽

Gene Families ◽

Pattern Recognition Receptors ◽

Molecular Evidence ◽

Immune Recognition ◽

Fig Wasp ◽

Fig Wasps ◽

Specific Domain ◽

Wasp Species ◽

Functional Studies

Pattern recognition receptors (PRRs) play important roles in detecting pathogens and initiating the innate immune response. Different evolutionary histories of pollinators and non-pollinators may result in different immune recognition systems. A previous study had reported that there were significant differences in peptidoglycan recognition proteins (PGRPs) between pollinators and non-pollinators in gene number and lineage of specific genes. In this study, based on the genomic data of 12 fig wasp species, with seven pollinators and five non-pollinators, we investigated the evolution patterns of PRRs, such as Gram-negative bacteria-binding proteins (GNBPs), C-type lectins (CTLs), scavenger receptors class B (SCRBs), fibrinogen-related proteins (FREPs), galectins, and thioester-containing proteins (TEPs). Our results showed that pollinators had no GNBP, but non-pollinators all had two gene members, which were clustered into two different clades in the phylogenetic tree, with each clade having specific domain and motif characteristics. The analysis of CTL and SCRB gene families also showed that there were lineage-specific genes and specific expansion in non-pollinators. Our results showed that there were significant differences in immune recognition between pollinators and non-pollinators, and we concluded that they had undergone flexible adaptive evolution in different environments. Our study can provide more molecular evidence for future functional studies on the immune system of fig wasps.

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Sexual Selection on Population-level Mating Opportunities Drives Morph Ratios in a Fig Wasp with Extreme Male Dimorphism

10.21203/rs.3.rs-98869/v1 ◽

2020 ◽

Author(s):

James M. Cook

Keyword(s):

Population Level ◽

Quantitative Prediction ◽

Fig Wasp ◽

Wing Polymorphism ◽

Fig Wasps ◽

Conditional Strategy ◽

Male Dimorphism ◽

Wasp Species ◽

Mating Opportunities ◽

Morph Ratios

Abstract Background Alternative 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 they obtain. Previously, we have shown qualitative support for this prediction across nine fig wasp species. Here I test the quantitative prediction in a population of the fig wasp Pseudidarnes minerva. In addition, while Hamilton envisaged simple Mendelian strategies, some fig wasp species with two wingless male morphs (but no winged males) show a conditional strategy with morph determination influenced by the number of wasps developing in a patch - I also test for this pattern in P. minerva. Results I 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. Conclusions Morph ratios in P. minerva are 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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The efficacy of natural selection in producing optimal sex ratio adjustments in a fig wasp species

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2020.1377 ◽

2020 ◽

Vol 287 (1934) ◽

pp. 20201377 ◽

Cited By ~ 1

Author(s):

Jaco M. Greeff ◽

Karina Pentz ◽

Marié Warren

Keyword(s):

Natural Selection ◽

Sex Ratio ◽

A Priori ◽

Fine Tuning ◽

Fig Wasp ◽

Fig Wasps ◽

Wasp Species ◽

Local Mate ◽

Sex Ratio Adjustment ◽

Dual Mechanism

Ever since Darwin's discovery of natural selection, we expect traits to evolve to increase organisms' fitness. As a result, we can use optimization models to make a priori predictions of phenotypic variation, even when selection is frequency-dependent. A notable example is the prediction of female-biased sex ratios resulting from local mate competition (LMC) and inbreeding. LMC models incorporate the effects of LMC and inbreeding. Fig wasp sex ratio adjustments fit LMC predictions well. However, the appropriateness of LMC models to fig wasps has been questioned, and the role that a coincidental by-product plays in creating the apparent fit has been clearly illustrated. Here, we show that the sex ratio adjustments of a fig wasp are the result of a dual mechanism. It consists of a standard facultative LMC response favoured by natural selection, as well as a mechanism that may be the result of selection, but that could also be a coincidental by-product. If it is a by-product, the fitness increase is coincidental and natural selection's role was limited to fine-tuning it for higher fitness returns. We further document a case of an apparent fitness-reducing sex ratio adjustment. We conclude that the use of the adaptationist approach demands that our understanding of traits must be remodelled continually to rectify spurious assumptions.

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The unknown followers: Discovery of a new species of Sycobia Walker (Hymenoptera: Epichrysomallinae) associated with Ficus benjamina L. (Moraceae) in the Neotropical region

Journal of Hymenoptera Research ◽

10.3897/jhr.67.29733 ◽

2018 ◽

Vol 67 ◽

pp. 85-102 ◽

Cited By ~ 3

Author(s):

Fernando Henrique Antoniolli Farache ◽

Cecilia Bernardo Pereira ◽

Cristiana Koschnitzke ◽

Levi Oliveira Barros ◽

Elmecelli Moraes de Castro Souza ◽

...

Keyword(s):

Native Species ◽

Ornamental Plants ◽

Neotropical Region ◽

Trophic Levels ◽

Fig Wasp ◽

Fig Wasps ◽

Wasp Species ◽

Fig Trees ◽

First Time ◽

A New Species

Biotic invasion in mutualistic communities is of particular interest due to the possible establishment of new relationships with native species. Ficus species are widely cultivated as ornamental plants, and they host specific communities of chalcid wasps that are strictly associated with the fig inflorescences. Some introduced fig species are capable of establishing new relationships with the local fig wasps, and fig wasp species may also be concomitantly introduced with their host plants. Ficusbenjamina L. is widely cultivated across the world, but the associated fig wasps are not reported outside of the species native range. We describe for the first time a non-pollinating fig wasp associated with F.benjamina inflorescences outside its native distribution. Sycobiahodites Farache & Rasplus, sp. n. is the third known species of the genus and was recorded in populations of F.benjamina introduced in the Neotropical region throughout several localities in Argentina, Brazil and Colombia. Sycobia is a gall-inducing non-pollinating fig wasp genus associated with fig trees in the Oriental and Australasian regions. This species competes with pollinators for oviposition sites and may hinder the future establishment of the native pollinator of F.benjamina, Eupristinakoningsbergeri Grandi, 1916 in the New World. However, the occurrence of a gall inducing species in this host plant may open ecological opportunities for the establishment of species belonging to other trophic levels such as cleptoparasite and parasitoid wasps.

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Molecular tools for understanding population structure in Antarctic species

Antarctic Science ◽

10.1017/s0954102000000353 ◽

2000 ◽

Vol 12 (3) ◽

pp. 288-296 ◽

Cited By ~ 7

Author(s):

Patrick M. Gaffney

Keyword(s):

Population Structure ◽

Sequence Data ◽

Rflp Analysis ◽

Pcr Primers ◽

Dna Polymorphisms ◽

Antarctic Species ◽

Mutation Scanning ◽

Patagonian Toothfish ◽

Species Specific ◽

Close Relatives

During the last decade, methods for detecting DNA polymorphisms have proliferated at a bewildering pace. Today the investigator must choose among various types of genetic markers as well as between a variety of methods for discovering and screening polymorphisms. Polymorphisms useful for the analysis of population structure are found in both mitochondrial and nuclear genomes. Marker development may proceed along two routes: 1) discovery of species–specific markers, and 2) application of universal methods. Species-specific markers are based on sequence data from the target species or close relatives, whereas universal markers are based on the use of polymerase chain reaction (PCR) primers targeted to regions highly conserved across diverse taxa. Markers commonly employed include mitochondrial DNA polymorphisms, microsatellites, anonymous nuclear loci and known genes (both coding and noncoding regions). Methods for detecting polymorphisms range from technically simple (RFLP analysis) to more sophisticated mutation scanning methods. We review the application of these approaches to several key Antarctic species (the Patagonian toothfish Dissostichus eleginoides, the mackerel icefish Champsocephalus gunnari, and the squid Martialia hyadesi Rochebrune & Mabille, 1889) and present preliminary data on genetic polymorphisms in toothfish and icefish.

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The population dynamics of a non-pollinating fig wasp on Ficus auriculata at Xishuangbanna, China

Journal of Tropical Ecology ◽

10.1017/s0266467405002634 ◽

2005 ◽

Vol 21 (5) ◽

pp. 581-584 ◽

Cited By ~ 12

Author(s):

Yan-Qiong Peng ◽

Da-Rong Yang ◽

Zhu-Biao Duang

Keyword(s):

Population Dynamics ◽

Fig Wasp ◽

Fig Wasps ◽

Male And Female ◽

Obligate Mutualism ◽

Species Specific ◽

Almost All

All fig wasps are confined to figs as larvae, and their specialized diets are restricted to fig embryos, galled fig ovaries or other fig wasp larvae (Boucek 1988). Almost all of the ∼800 Ficus species (Moraceae) are involved in species-specific obligate mutualism with a pollinating fig wasp (Hymenoptera: Agaonidae), which also strictly depends on its host fig for reproduction (Berg 2003, Ramirez 1970, Wiebes 1979). More than half of all fig species are functionally dioecious, with male and female functions relegated to separate plants, called gall and seed figs (Kjellberg et al. 1987). Gall figs are functionally male because they foster the pollinator larvae that disperse the fig's pollen as adults. Seed figs are functionally female and produce only seeds. The styles are too long for pollinator ovipositors to reach the ovules, and hence they cannot lay eggs. Gall fig styles are short (Ganeshaiah et al. 1995, Weiblen et al. 1995).

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Fighting injuries, fig exit, and dimorphism in two species of sycoryctine fig wasp (Chalcidoidea, Pteromalidae)

Journal of Hymenoptera Research ◽

10.3897/jhr.74.36461 ◽

2019 ◽

Vol 74 ◽

pp. 105-121

Author(s):

Da-Mien Wong ◽

Anthony Bain ◽

Shiuh-Feng Shiao ◽

Lien-Siang Chou

Keyword(s):

Mating Strategies ◽

Exit Rate ◽

Behavioral Differences ◽

Fig Wasp ◽

Fig Wasps ◽

Wasp Species ◽

Invertebrate Species ◽

Fig Tree

Similar to many vertebrate and invertebrate species, many fig wasp species are fighting other members of their species for mates. Fighting between the males of many non-pollinating fig wasp species involves injuries and fatalities. Studies have shown that large males fight for mates, whereas conspecific small males tend to adopt nonfighting, sneaky behaviors. To analyze male morphs in two non-pollinating fig wasps (Philotrypesis taida Wong & Shiao, 2018 and Sycorycteridea taipeiensis Wong & Shiao, 2018) associated with the fig tree Ficus benguetensis, the head and mandible allometry and injuries were examined as well as the morphologies of their heads and mandibles. Male fig wasps of these two nonpollinating species can be divided into two morphological groups according to their head and mandible shapes. Approximately 88% of the Philotrypesis and 62% of the Sycorycteridea males were injured and no males belonging to largest morphs were decapitated. Moreover, nearly 31% of the Philotrypesis and 45% of the Sycorycteridea males left their natal figs. No difference in injury level or male exit rate between the male morphs was observed. This study reveals slight morphological and behavioral differences that may hint towards different mating strategies among morphs.

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Community Structure and Undescribed Species Diversity in Non-Pollinating Fig Wasps Associated with the Strangler Fig Ficus petiolaris

Insect Systematics and Diversity ◽

10.1093/isd/ixaa005 ◽

2020 ◽

Vol 4 (2) ◽

Author(s):

Jordan D Satler ◽

Kristen K Bernhard ◽

John O Stireman ◽

Carlos A Machado ◽

Derek D Houston ◽

...

Keyword(s):

Community Structure ◽

Species Diversity ◽

Niche Partitioning ◽

Morphological Data ◽

Fig Wasp ◽

Ecological Data ◽

Fig Wasps ◽

Wasp Species ◽

Mixed Support ◽

Growing Body

Abstract Figs and their associated mutualistic and parasitic wasps have been a focus of intensive ecological and evolutionary research due to their diversity, unusual reproductive biology, and highly coevolved interspecific relationships. Due to the ecological dependence of their interactions, fig wasps were once considered to be fig-species specific and to cospeciate with their hosts, however, a growing body of evidence reveals mixed support for species specificity and the importance of additional evolutionary processes (e.g., host switching) structuring these long-term interactions. Our research on the genus Idarnes Walker, 1843 (Hymenoptera, Agaonidae), a common non-pollinating wasp of New World fig flowers, reveals a community in which multiple wasp species coexist on the same host in space and time. Using both molecular and morphological data, we identify five distinct Idarnes lineages associated with a single host fig species, Ficus petiolaris Kunth, 1817 (Rosales, Moraceae). A comprehensive phylogenetic analysis including Idarnes species from numerous host fig species reveals that the lineages associated with F. petiolaris do not form a monophyletic group but are distantly related, suggesting multiple independent colonization events and subsequent diversification. Morphological and ecological data provide support that the wasps are partitioning niches within the figs, explaining the coexistence of these diverse lineages on the same host fig. These results, coupled with a growing body of research on pollinating and non-pollinating fig wasps, bring into focus a more dynamic picture of fig and fig wasp coevolution and highlight how wasp lineage divergence and niche partitioning contributes to increased species diversity and community structure on a single fig host.

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Two levels of host-specificity in a fig-associated Caenorhabditis

10.1101/261958 ◽

2018 ◽

Author(s):

Gavin C. Woodruff ◽

Patrick C. Phillips

Keyword(s):

Natural History ◽

Host Specificity ◽

Evolutionary Biology ◽

Interspecific Interactions ◽

Biotic Interactions ◽

Close Relative ◽

Fig Wasp ◽

Fig Wasps ◽

C Elegans ◽

Functional Genetics

AbstractBackgroundBiotic interactions are ubiquitous and require information from ecology, evolutionary biology, and functional genetics in order to be completely understood. However, study systems that are amenable to investigations across such disparate fields are rare. Figs and fig wasps are a classic system for ecology and evolutionary biology with poor functional genetics; C. elegans is a classic system for functional genetics with poor ecology. In order to help bridge these disciplines, here we describe the natural history of a close relative of C. elegans, C. sp. 34, that is associated with the fig Ficus septica and its pollinating Ceratosolen wasps.ResultsTo understand the natural context of fig-associated Caenorhabditis, fresh F. septica figs from four Okinawan islands were sampled, dissected, and observed under microscopy. C. sp. 34 was found in all islands where F. septica figs were found. C. sp. 34 was routinely found in the fig interior and almost never observed on the outside surface. Caenorhabditis was only found in pollinated figs, and C. sp. 34 was more likely to be observed in figs with more foundress pollinating wasps. Actively reproducing C. sp. 34 dominated younger figs, whereas older figs with emerging wasp progeny harbored C. sp. 34 dispersal larvae. Additionally, C. sp. 34 was observed dismounting from plated Ceratosolen pollinating wasps. C. sp. 34 was never found on non-pollinating, parasitic Philotrypesis wasps. Finally, C. sp. 34 was only observed in F. septica figs among five Okinawan Ficus species sampled.ConclusionThese observations suggest a natural history where C. sp. 34 proliferates in young F. septica figs and disperses from old figs on Ceratosolen pollinating fig wasps. The fig and wasp host specificity of this Caenorhabditis is highly divergent from its close relatives and frames hypotheses for future investigations. This natural co-occurrence of the fig/fig wasp and Caenorhabditis study systems sets the stage for an integrated research program that can help to explain the evolution of interspecific interactions.

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Genome-Wide Analysis of Peptidoglycan Recognition Protein Genes in Fig Wasps (Hymenoptera, Chalcidoidea)

Insects ◽

10.3390/insects11090597 ◽

2020 ◽

Vol 11 (9) ◽

pp. 597

Author(s):

Hong-Xia Hou ◽

Meng-Yuan Guo ◽

Jin Geng ◽

Xian-Qin Wei ◽

Da-Wei Huang ◽

...

Keyword(s):

Innate Immunity ◽

Recognition System ◽

Molecular Evidence ◽

Signal Pathways ◽

Immune Recognition ◽

Toll Pathway ◽

Fig Wasp ◽

Fig Wasps ◽

Evolutionary Patterns ◽

Wasp Species

The innate immunity is the most important defense against pathogen of insects, and the peptidoglycan recognition proteins (PGRPs) play an important role in the processes of immune recognition and initiation of Toll, IMD and other signal pathways. In fig wasps, pollinators and non-pollinators present different evolutionary histories and lifestyles, even though both are closely associated with fig syconia, which may indicate their different patterns in the evolution of PGRPs. By manual annotation, we got all the PGRP genes of 12 fig wasp species, containing seven pollinators and five non-pollinators, and investigated their putative different evolutionary patterns. We found that the number of PGRP genes in pollinators was significantly lower than in non-pollinators, and the number of catalytic PGRP presented a declining trend in pollinators. More importantly, PGRP-SA is associated with initiating the Toll pathway, as well as gram-negative bacteria-binding proteins (GNBPs), which were completely lost in pollinators, which led us to speculate that the initiation of Toll pathway was simpler in pollinators than in non-pollinators. We concluded that fig pollinators owned a more streamlined innate immune recognition system than non-pollinators. Our results provide molecular evidence for the adaptive evolution of innate immunity in insects of host specificity.

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