‘Shouldering’ exaggerated genitalia: a unique behavioural adaptation for the retraction of the elongate intromittant organ by the male rove beetle (Aleochara tristis Gravenhorst)

Abstract

Complex genitalia are ubiquitous among arthropods, but little attention has been given to the fact that the evolution of such elaborate structures may have led to biomechanical constraints that hinder their usage. In the rove beetle, Aleochara tristis, the male's intromittant organ consists of a long flagellum that is more than twice the body length. It is introduced into the spermathecal duct of the female during copulation. The flagellum apparently functions as a guiding rod for a tube growing from the spermatophore that the male deposits in the female's genital chamber. The extraordinary length of the intromittant organ poses a unique physical challenge for the male. During its retraction from the female after mating, the flagellum is under considerable tension. Any sudden release of this tension would result in the flagellum becoming severely entangled, preventing the male from mating again. In response to this novel physical challenge, males have apparently evolved a specialized behavioural adaptation that prevents entanglement after copulation. While retracting the flagellum from the female, the male secures it between a wing shoulder and the pronotum ('shouldering'), holding it taut for about one half of its length. This allows the stepwise retraction of the flagellum from the female and allows it to be retracted back into the male's body in an orderly fashion. This is, to our knowledge, the first demonstration of a behavioural adaptation that has evolved to ameliorate the biomechanical problems caused by exaggerated genital morphology.

Experimental reduction of intromittent organ length reduces male reproductive success in a bug

“…Such an extremely long male intromittent organ is common in the Heteroptera [26 -28], and is also found in several other insect groups including the Coleoptera [15,16,29,30], Dermaptera [31,32] and Zoraptera [22]. A previous correlational study in L. simulans found stabilizing post-copulatory selection on processus length: males with an average processus length were most likely to inseminate a female [33].…”

Insertion and withdrawal of extremely elongated genitalia: a simple mechanism with a highly modified morphology in the leaf beetle, Lema coronata

“…How do males with extremely elongated genitalia overcome this problem? For example, the male rove beetle Aleochara tristis Gravenhorst secures its long genital tube between the wing shoulder and the pronotum when the tube is held strained at approximately one‐half of its length during genital withdrawal from the female (Gack & Peschke, 2005). In another case, the male fly Ceratitis capitata (Wiedemann) folds the basal portion of his distiphallus backward and inserts the distiphallus into a female from the folded portion (Eberhard, 2005).…”

“…The elongated MEG is inserted into the spermathecal duct during copulation (Matsumura & Akimoto, 2009), although the mechanisms of its insertion and withdrawal are unknown. The mating behaviour is simple in L. coronata (Matsumura & Akimoto, 2009), in contrast to the highly specialized mating behaviour of the rove beetle (Gack & Peschke, 2005). To understand how L. coronata deals with extremely elongated genitalia, we investigated the morphology of the internal sac, behaviour, and the genital mesh.…”

Male genital size reflects a tradeoff between attracting mates and avoiding predators in two live-bearing fish species

“…Postmating sexual selection can result from several mechanisms, such as sperm competition, cryptic female choice, or sexual conflict over fertilization decisions (1)(2)(3)(4)(5)(6)(7)(8). Although much of the current research in this field centers around the postmating sexual selection hypothesis, there are two alternative ideas that have received comparatively little investigation: premating sexual selection and natural selection on males (9)(10)(11)(12).…”