American Society of Naturalists

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“Macroevolutionary origin and adaptive function of a polymorphic female signal involved in sexual conflict”

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Beatriz Willink, M. Catherine Duryea, and Erik I. Svensson (Nov 2019)

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Developmental color signals in female-polymorphic damselflies exploit male biases and reduce premature mating attempts

Female damselflies have evolved developmentally dynamic color signals to reduce premature male-mating attempts

Mating wheel of the common Bluetail damselfly (<i>Ischnura elegans</i>). The male and male-mimicking female are nearly identical in coloration.<br/>(Credit: E. I. Svensson)
Mating wheel of the common Bluetail damselfly (Ischnura elegans). The male and male-mimicking female are nearly identical in coloration.
(Credit: E. I. Svensson)

Evolutionary biologists have studied male color signals for decades and asked how this variation influences male mating success. The occurrence of conspicuous color signals in females constitutes somewhat of a paradox, as in most species females are unlikely to compete for mating opportunities with males.

Many species of pond damselflies in the genus Ischnura have two or three heritable female color morphs that are not present in the monomorphic males. Females belonging to one of the morphs typically resemble males in their color pattern, and are thought to be “male mimics”. Because superfluous male-mating attempts are costly to females, male mimics might benefit if their male-like appearance reduces the rate by which males approach them. The other female morph(s) are termed “heterochromatic females” and are more easily recognized as potential mates by males. Heterochromatic females may suffer greater costs from unsought mating attempts, particularly prior to female sexual maturity. Willink et al. asked if developmental color changes in heterochromatic females could protect them from male-induced harm, by reducing the number of male-mating attempts.

Through field observations of one focal species (the common bluetail damselfly, Ischnura elegans), Willink et al. showed that sexually-immature heterochromatic females express a bright abdomen color patch that is also present in males and male-mimics of all ages. However, as heterochromatic females become sexually mature, their color patch is covered with darker pigment. Experimental manipulations of the color patch showed that heterochromatic females with immature coloration were approached less often by males than seemingly older females were. This experimental manipulation suggests that the bright color patch serves an adaptive anti-harassment function. Willink et al. further performed a phylogenetic comparative analysis of female color changes across the genus Ischnura. They demonstrate that this immature signal has evolved multiple times in heterochromatic females, but only in the presence of male-mimics. The combination of experimental and comparative approaches in this study therefore suggest that antagonistic inter-sexual interactions during development has driven the evolution of color signals in females.


Abstract

Inter-sexual 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 I. elegans, males and male-mimicking females express a blue abdominal patch throughout post-emergence life. Using phenotypic manipulations we show that the developmental expression of this signalling trait in heterochrome females reduces pre-mating harassment prior to sexual maturity. Across species, this signal evolved repeatedly, but in heterochrome females, its origin is contingent upon 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 anti-harassment function has a key role in sexual conflict driven by pre-mating interactions.