Fitness advantages of the biased use of paired laterally symmetrical penises in an insect

Abstract

The evolution of laterality, that is the biased use of laterally paired, morphologically symmetrical organs, has attracted the interest of researchers from a variety of disciplines. It is, however, difficult to quantify the fitness benefits of laterality because many organs, such as human hands, possess multimodal functions. Males of the earwig Labidura riparia (Insecta: Dermaptera: Labiduridae) have morphologically similar laterally paired penises, only one of which is used for inseminating the female during a single copulation bout, and thus provide a rare opportunity to address how selection pressure may shape the evolution of population‐level laterality. Our population studies revealed that in 10 populations, located at 2.23–43.3° north, the right penis is predominantly used for copulating (88.6%). A damaged penis was found in 23% of rare left‐handers, suggesting that the left penis can function as a spare when the right one is damaged. By pairing L. riparia females with surgically manipulated males, we found that males forced to use the right penis outperformed left‐handed males in copulation (the probability of establishing genital coupling during the 1‐hr observation period: odds ratio [OR] of 3.50) and insemination (probability of transferring a detectable amount of sperm: OR of 2.94). This right‐handed advantage may be due to the coiled morphology of the sperm storage organ with a right‐facing opening. Thus, female genital morphology may play a significant role in the evolution of handedness and may have acted as a driving force to reduce penis number in related taxa.

Genetic assimilation and the evolution of direction of genital asymmetry in anablepid fishes

“…In anablepid fishes, sidedness evolved consistently in one direction (i.e. left-sided males became more abundant or fixed), and the same was observed for earwigs [72,75,76]. However, in phallostethid fishes, entirely right-sided as well as entirely left-sided species evolved [74,77].…”

“…J. darwini and J. luxata ) are also left-biased (electronic supplementary material, table S1). Alternatively, there could be fitness advantages of one morph over the other due to correlated traits or constraints [72]. This topic warrants further investigation.…”

A new species of Diplatys (Insecta, Dermaptera, Diplatyidae) earwig from the Western Ghats of India

“…However, in this species, a recurved flange at the virgal tip is considered responsible for sperm removal ( Kamimura 2000 ). Although males of most earwig species directly insert a virga into the female spermatheca for transferring sperm during copulation ( Kamimura 2014 ; Kamimura et al 2019 ), D. flavicollis is an exception: the virgal tips are much wider than the spermathecal openings and ducts, indicating that physical removal of stored sperm by a virga is not feasible ( Kamimura 2004 ). However, as in males, female genitalia are quite variable among diplatyid species ( Popham 1965 ; Klass 2003 ).…”

No evidence for asymmetric sperm deposition in a species with asymmetric male genitalia

“…Asymmetric genitalia are observed in many species and must have recurrently evolved from symmetric ancestors ( Huber, Sinclair & Schmitt, 2007 ; Huber, 2010 ; Schilthuizen, 2013 ). They have been associated with a specific interlocking of female and male genitalia ( Kamimura, Yang & Lee, 2019 ; Holwell et al, 2015 ; Rhebergen et al, 2016 ; Richmond, Park & Henry, 2016 ) and with lateralized courtship and copulation behavior ( Rhebergen et al, 2016 ; Orbach et al, 2020 ; Torres-Dowdall et al, 2020 ). However, the ultimate evolutionary cause for these transitions from symmetry to asymmetry are not fully understood ( Schilthuizen, 2013 ).…”