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

Abstract

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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“…This is not surprising, considering that the floral forms of this polyphenic species switch between two extremes (G omez et al, 2020). Plasticity-mediated movements across the morphospace have been reported for several other organisms (Pfennig, 2021), like fish (Muschick et al, 2011;Lofeu et al, 2021), ants (Oettler et al, 2019), nematodes (Susoy et al, 2015) and even plants (Barnett et al, 2018). Our case is remarkable because, in contrast to the findings of b) Floral disparity between each of the two phenotypes (i.e.…”

From egg to adult: a developmental table of the antMonomorium pharaonis

“…Queen and worker castes display dramatic differences in morphology and life history, the key features being wing polyphenism, comprising of winged queens and wingless workers; a morphological and reproductive asymmetry between queen and worker castes; and within the worker caste, the evolution of soldiers. Each of these innovations evolved through the differential regulation of the genetic toolkit among castes during preimaginal stages of development (Dewitz 1878, Wheeler and Nijhout 1981, Wheeler 1986, Abouheif and Wray 2002, Wheeler 2003, Sameshima et al 2004, Gotoh et al 2005, Khila and Abouheif 2008, Khila and Abouheif 2010, Rajakumar et al 2012, Gotoh et al 2016, Béhague et al 2018, Oettler et al 2019. Furthermore, within ant societies developing larvae play fundamental roles in colony-level regulation.…”

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