Wing reduction influences male mating success but not female fitness in cockroaches

Abstract

Although cockroaches (Blattodea s. str.) exhibit high proportion of species with reduced wings, the underlying evolutionary forces remain unclear. Wing reduction in insects is generally considered advantageous for females and a trade-off between investment into the flying apparatus and reproduction is predicted to explain its evolution. However, what if the wing maintenance is an important issue for males’ fitness? Males raise wings during the ritualized courtship which is viewed as an unavoidable movement unveiling the tergal glands for female access. We, however, propose a novel male mating success hypothesis suggesting that male wings are essential for their successful mating. We tested these two competing, but not mutually exclusive hypotheses in the cockroach Eublaberus distanti. We found no effect of female wing loss on any of the measured fecundity characteristics despite that alatectomized females histolyzed flight muscles. On the contrary, alatectomized males did not histolyze wing muscles, but experienced a markedly decreased mating success. Our findings, therefore, provide the first evidence on the crucial mechanical role of wings on male mating success. Consequently, selection for the retention of wings in males rather than for their reduction in females can explain the evolution of sexual wing dimorphism in cockroaches and other insects.

Evolution of wing polymorphism and genital asymmetry in the thread‐legged bugs of the tribe Metapterini Stål (Hemiptera, Reduviidae, Emesinae) based on morphological characters

“…The sexually dimorphic condition found in B. brachmanni , in which females are apterous and males macropterous, is congruent with the idea that flightless females invest these resources in reproduction and not flight (Roff & Fairbairn, 1991; Kotyk & Varadínová, 2017). A more intriguing question is why a transition to a fully apterous condition happened in both sexes of some genera, such as in the genera of clade J.…”

A second view on the evolution of flight in stick and leaf insects (Phasmatodea)

“…As a consequence, flightless taxa may show increased fecundity because resources previously invested in maintaining the energetically costly flight apparatus can now be allocated to reproduction [ 6 , 15 , 16 ]. The underlying trade-off between dispersal and reproduction has been repeatedly demonstrated for females [ 17 – 21 ] and males [ 22 – 24 ], albeit the loss of flight is generally more common in females, often resulting in wing dimorphic species with volant males [ 1 , 6 , 25 ]. In some species, the dilemma of dispersal capability versus fecundity is solved by wing polyphenism, where an either winged or flightless phenotype is adopted in response to specific environmental triggers [ 1 , 16 , 18 , 26 – 29 ].…”

Proper direction of male genitalia is prerequisite for copulation in Drosophila, implying cooperative evolution between genitalia rotation and mating behavior

“…Upon an alteration in body structure, mating behaviors are also found to be inflexible in other insects. For example, the South American four spot-roach, Eublaberus distanti has a highly ritualized mating behavior, which requires male wing rise 27 . Males in which the wings have been partially or completely surgically removed still perform the full sequence of mating behaviors and complete their courtship ritual 27 .…”

“…For example, the South American four spot-roach, Eublaberus distanti has a highly ritualized mating behavior, which requires male wing rise 27 . Males in which the wings have been partially or completely surgically removed still perform the full sequence of mating behaviors and complete their courtship ritual 27 . Therefore, in cases in which a particular body structure and mating behavior are cooperatively required to achieve successful mating, the mating behavior is often inflexible to adjust to a change in body structure, as found here for the dorsoventral direction of the male genitalia.…”