Macroevolutionary Origin and Adaptive Function of a Polymorphic Female Signal Involved in Sexual Conflict

Abstract

Intersexual signals that reveal developmental or mating status in females have evolved repeatedly in many animal lineages. Such signals have functions in sexual conflict over mating and can therefore influence sexually antagonistic coevolution. However, we know little about how female signal development modifies male mating harassment and thereby sexual conflict. Here, we combine phylogenetic comparative analyses of a color polymorphic damselfly genus (Ischnura) with behavioral experiments in one target species to investigate the evolutionary origin and current adaptive function of a developmental female color signal. Many Ischnura species have multiple female color morphs, which include a male-colored morph (male mimics) and one or two female morphs that differ markedly from males (heterochrome females). In Ischnura elegans, males and male-mimicking females express a blue abdominal patch throughout postemergence life. Using phenotypic manipulations, we show that the developmental expression of this signaling trait in heterochrome females reduces premating harassment prior to sexual maturity. Across species this signal evolved repeatedly, but in heterochrome females its origin is contingent on the signal expressed by co-occurring male-mimicking females. Our results suggest that the co-option of a male-like trait to a novel female antiharassment function plays a key role in sexual conflict driven by premating interactions.

Temperature drives pre‐reproductive selection and shapes the biogeography of a female polymorphism

“…Female morphs in I. elegans and other taxa often differ in multiple traits apart from colour, including thermal physiology, fecundity, behaviour and parasite loads (Gosden & Svensson ; Lancaster et al ; Willink & Svensson ). For instance, the male mimic has lower fecundity than the two gynochrome female morphs (Willink et al ), which could reflect costs of mimicry due to the more male like shape of these male mimics (Gosden & Svensson ). The lower fecundity of the male mimic could also be a cost of their earlier sexual maturity and faster colour development that we have demonstrated in this study (Fig.…”

“…1) (Cordero et al 1998;Svensson et al 2009). Female colour maturation is tightly correlated with female reproductive maturity, as immature-coloured females of all morphs have high levels of reproductive failure and lay few eggs, if any at all, if given the opportunity (Willink et al 2019a).…”

Changes in gene expression during female reproductive development in a colour polymorphic insect

“…This adaptive colour change in A-females is consistent with male mimicry, by which A-females avoid excessive and costly male-mating harassment Gering 2017). In contrast, the violet thorax colour of I-females becomes greenish-brown in association with increased reproductive output (Willink et al 2019;Fig. 1b).…”

“…1a). Female morphs differ in both their sexually mature (final) colour patterns as well as in the qualitative colour changes that are expressed during sexual development (Cordero et al 1998;Svensson et al 2009;Willink et al 2019;Fig. 1 Previous studies using breeding experiments in controlled laboratory environments across multiple generations have revealed that colour morph development is governed by a single autosomal locus (or a set of tightly linked loci) with sex-limited expression to females (Cordero 1990;Sánchez-Guillén et al 2005).…”

“…Two of the female morphs in I. elegans differ phenotypically from males in their sexually mature colouration, while the third morph is considered to be a male-mimic, with a colour pattern strikingly similar to that of males ). Male-mimicking females also differ from the other two morphs in their ontogenetic trajectories of colour change and in several other phenotypic traits, including fecundity Willink et al 2019), mating rates ), parasite resistance and tolerance (Willink and Svensson 2017), cold tolerance (Lancaster et al 2017) and adult development times (Svensson et al 2020). Some of these phenotypic differences between the morphs are likely to be adaptive and a result of correlational selection (Svensson 2017).…”