Seasonal polyphenism in wing coloration affects species recognition in rubyspot damselflies (Hetaerina spp.)

Abstract

Understanding how phenotypic plasticity evolves and in turn affects the course of evolution is a major challenge in modern biology. By definition, biological species are reproductively isolated, but many animals fail to distinguish between conspecifics and closely related heterospecifics. In some cases, phenotypic plasticity may interfere with species recognition. Here, we document a seasonal polyphenism in the degree of dark wing pigmentation in smoky rubyspot damselflies (Hetaerina titia) -a shift so pronounced that it led early researchers to classify different forms of H. titia as separate species. We further show how the seasonal colour shift impacts species recognition with the sympatric congener Hetaerina occisa. Interspecific aggression (territorial fights) and reproductive interference (mating attempts) are much more frequent early in the year, when H. titia more closely resembles H. occisa, compared to later in the year when the dark phase of H. titia predominates. Using wing colour manipulations of tethered damselflies, we show that the seasonal changes in interspecific interactions are caused not only by the seasonal colour shift but also by shifts in discriminatory behaviour in both species. We also experimentally tested and rejected the hypothesis that learning underlies the behavioural shifts in H. occisa. An alternative hypothesis, which remains to be tested, is that the seasonal polyphenism in H. titia wing coloration has resulted in the evolution of a corresponding seasonal polyphenism in species recognition in H. occisa. This study illustrates one of the many possible ways that plasticity in species recognition cues may influence the evolution of interspecific interactions.

Why are female color polymorphisms rare in territorial damselflies?

“…One person presented the tethered female while a second person recorded the male's responses. Females were tethered with fine transparent thread (0.076 mm diameter) to a thin fiberglass pole and directed to fly within 1 m of the male for 5 s or until the male stopped interacting with her, whichever happened last (as in Drury et al., ). We used unmanipulated females as the control group, for lack of a suitable sham manipulation treatment (any paint added to a female's abdomen could affect her appearance).…”

“…The possible responses of males were as follows: no response (remained perched); approach (flew toward the female); clasp (clasped the female with his cerci); attempted clasp (approached the female with abdomen curled into a clasping position but did not clasp the female); slam (rammed into the female headfirst); and grab (grasped the female with his legs). Slams and grabs are aggressive responses, frequently seen in male territorial fights (Anderson & Grether, ), while clasps and attempted clasps are sexual responses (Drury et al., ). Approaches are a necessary prelude to both kinds of physical interactions and were not classified as aggressive or sexual.…”

“…A “successful” test was defined, a priori, as one in which the male responded sexually to at least one of the three females presented, regardless of the female's treatment group (Drury et al., ). At Quebrada Socorro, 31 of 50 tests were successful; at Rio Tempisquito, 39 of 53 tests were successful.…”

“…The goal of our experiment was to test the alternative hypothesis that males respond too indiscriminately for frequency‐dependent male mating harassment to arise in the first place. There is ample evidence for indiscriminate male mate recognition in Hetaerina ; males of most species tested do not discriminate between conspecific females and females of sympatric congeners (Drury, Anderson, & Grether, ). However, the differences in coloration between the females of most sympatric Hetaerina species are subtler than the differences between the morphs of species with female polymorphisms.…”

Molecular Mechanisms Underlying Color Vision and Color Formation in Dragonflies

“…17.1g, h), sex-specific color formation is regulated cell-autonomously in dragonflies. In many dragonfly species, adult body color plays important roles in partner recognition (Corbet 1999;Svensson et al 2007;Córdoba-Aguilar 2008;Svensson et al 2014;Takahashi et al 2014;Beatty et al 2015;Drury et al 2015). Interspecific or male-male connection has sometimes been observed in the field between similar-colored individuals , and interspecific hybrids has been reported occasionally (Corbet 1999;Futahashi 1999;Futahashi and Futahashi 2007;Moriyasu and Sugimura 2007;Ozono et al 2012;Sánchez-Guillén et al 2014;Futahashi 2016a).…”