Evolution of Social Insect Polyphenism Facilitated by the Sex Differentiation Cascade

Klein, Antonia; Schultner, Eva; Lowak, Helena; Schrader, Lukas; Heinze, Juergen; Holman, Luke; Oettler, Jan

doi:10.1371/journal.pgen.1005952

Cited by 54 publications

(58 citation statements)

References 61 publications

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“…temperature and nutrition) or genetic (e.g. sex chromosomes and genetic caste determination) factors leading to development of alternative phenotypic states (Brian, 1979;Anderson et al, 2008;Schwander et al, 2010;Bopp et al, 2014;Klein et al, 2016). However, caste development is more frequently mediated by environmental factors, whereas sex development is more frequently mediated by genetic factors.…”

Section: Discussionmentioning

confidence: 99%

Caste development and evolution in ants: it's all about size

Trible

Kronauer

2017

Journal of Experimental Biology

101

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Female ants display a wide variety of morphological castes, including workers, soldiers, ergatoid (worker-like) queens and queens. Alternative caste development within a species arises from a variable array of genetic and environmental factors. Castes themselves are also variable across species and have been repeatedly gained and lost throughout the evolutionary history of ants. Here, we propose a simple theory of caste development and evolution. We propose that female morphology varies as a function of size, such that larger individuals possess more queen-like traits. Thus, the diverse mechanisms that influence caste development are simply mechanisms that affect size in ants. Each caste-associated trait has a unique relationship with size, producing a phenotypic space that permits some combinations of worker-and queen-like traits, but not others. We propose that castes are gained and lost by modifying the regions of this phenotypic space that are realized within a species. These modifications can result from changing the sizefrequency distribution of individuals within a species, or by changing the association of tissue growth and size. We hope this synthesis will help unify the literature on caste in ants, and facilitate the discovery of molecular mechanisms underlying caste development and evolution.

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Section: Discussionmentioning

confidence: 99%

Caste development and evolution in ants: it's all about size

Trible

Kronauer

2017

Journal of Experimental Biology

101

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“…Ants of the genus Cardiocondyla are exceptional in their extent of realized phenotypic plasticity. Therefore, they provide a promising model for dissecting molecular and genomic differences underlying the evolution of novel developmental switches through genetic accommodation, both within and between closely related species (Klein et al, ; Schrader et al, ; Schrader, Helanterä, & Oettler, ). Our study is only the first step towards uncovering these molecular differences.…”

Section: Discussionmentioning

confidence: 99%

“…At the developmental and genetic level, Klein et al () showed that wing polyphenism in males and females in C. obscurior evolved through co‐option of ancestral sex‐differentiation pathways (including the terminal sex differentiation transcription factor doublesex ), which is known to control a large suite of developmental toolkit genes. Furthermore, an initial RNAseq study on early third instar larvae of C. obscurior showed a large morph‐specific gene expression bias, and in particular, that wingless male at this stage are characterized by an enriched expression of genes associated with larval and imaginal disc development (Schrader et al, ).…”

Section: Introductionmentioning

confidence: 99%

Interruption points in the wing gene regulatory network underlying wing polyphenism evolved independently in male and female morphs in Cardiocondyla ants

et al. 2018

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Wing polyphenism in ants, which produces a winged female queen caste and a wingless female worker caste, evolved approximately 150 million years ago and has been key to the remarkable success of ants. Approximately 20 million years ago, the myrmicine ant genus Cardiocondyla evolved an additional wing polyphenism among males producing two male morphs: wingless males that fight to enhance mating success and winged males that disperse. Here we show that interruption of rudimentary wing‐disc development in larvae of the ant Cardiocondyla obscurior occurs further downstream in the network in wingless males as compared with wingless female workers. This pattern is corroborated in C. kagutsuchi, a species from a different clade within the genus, indicating that late interruption of wing development in males is conserved across Cardiocondyla. Therefore, our results show that the novel male wing polyphenism was not developmentally constrained by the pre‐existing female wing polyphenism and evolved through independent alteration of interruption points in the wing gene network. Furthermore, a comparison of adult morphological characters in C. obscurior reveals that developmental trajectories lead to similar morphological trait integration between winged and wingless females, but dramatically different integration between winged and wingless males. This suggests that the alternative sex‐specific developmental routes to achieve winglessness in the genus Cardiocondyla may have evolved through different selection regimes acting on wingless males and females.

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“…Neither brother-sister mating nor mother-son mating lead to the production of diploid males [57,58], suggesting that Cardiocondyla has evolved an alternative to sl-CSD. A recent study documented sex-specific splicing of transformer, a key player in insect sex determination, but it is still unclear what initially triggers the development of males from unfertilized eggs and females from fertilized eggs [59]. In C. obscurior, experimental siblingmating over 10 generations resulted in fitness decreases, such as shortened queen lifespan, higher brood mortality and more strongly male-biased sex ratios [57].…”

Section: (A) Queen Number and Morphologymentioning

confidence: 99%

Life-history evolution in ants: the case ofCardiocondyla

Heınze¹

2017

Proc. R. Soc. B.

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Ants are important components of most terrestrial habitats, and a better knowledge of the diversity of their life histories is essential to understand many aspects of ecosystem functioning. The myrmicine genus Cardiocondyla shows a wide range of colony structures, reproductive behaviours, queen and male lifespans, and habitat use. Reconstructing the evolutionary pathways of individual and social phenotypic traits suggests that the ancestral life history of Cardiocondyla was characterized by the presence of multiple, short-lived queens in small-sized colonies and a male polyphenism with winged dispersers and wingless fighters, which engage in lethal combat over female sexuals within their natal nests. Single queening, queen polyphenism, the loss of winged males and tolerance among wingless males appear to be derived traits that evolved with changes in nesting habits, colony size and the spread from tropical to seasonal environments. The aim of this review is to bring together the information on life-history evolution in Cardiocondyla and to highlight the suitability of this genus for functional genomic studies of adaptation, phenotypic plasticity, senescence, invasiveness and other key life-history traits of ants.

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Evolution of Social Insect Polyphenism Facilitated by the Sex Differentiation Cascade

Cited by 54 publications

References 61 publications

Caste development and evolution in ants: it's all about size

Caste development and evolution in ants: it's all about size

Interruption points in the wing gene regulatory network underlying wing polyphenism evolved independently in male and female morphs in Cardiocondyla ants

Life-history evolution in ants: the case ofCardiocondyla

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