Correlated evolution between targets of pre‐ and postcopulatory sexual selection across squamate reptiles

Abstract

Sexual selection reflects the joint contributions of precopulatory selection, which arises from variance in mating success, and postcopulatory selection, which arises from variance in fertilization success. The relative importance of each episode of selection is variable among species, and comparative evidence suggests that traits targeted by precopulatory selection often covary in expression with those targeted by postcopulatory selection when assessed across species, although the strength and direction of this association varies considerably among taxa. We tested for correlated evolution between targets of pre‐ and postcopulatory selection using data on sexual size dimorphism (SSD) and testis size from 151 species of squamate reptiles (120 lizards, 31 snakes). In squamates, male–male competition for mating opportunities often favors large body size, such that the degree of male‐biased SSD is associated with the intensity of precopulatory selection. Likewise, competition for fertilization often favors increased sperm production, such that testis size (relative to body size) is associated with the intensity of postcopulatory selection. Using both conventional and phylogenetically based analyses, we show that testis size consistently decreases as the degree of male‐biased SSD increases across lizards and snakes. This evolutionary pattern suggests that strong precopulatory selection may often constrain the opportunity for postcopulatory selection and that the relative importance of each selective episode may determine the optimal resolution of energy allocation trade‐offs between traits subject to each form of sexual selection.

Population density and structure drive differential investment in pre- and postmating sexual traits in frogs

“…Such a negative relationship between pre-and postmating investment across species has been reported in several recent comparative studies (Poulin and Morand 2000;Fitzpatrick et al 2012;Lüpold et al 2014;Dines et al 2015;Kahrl et al 2016). Such a negative relationship between pre-and postmating investment across species has been reported in several recent comparative studies (Poulin and Morand 2000;Fitzpatrick et al 2012;Lüpold et al 2014;Dines et al 2015;Kahrl et al 2016).…”

“…The gradual shift in the covariance between pre-and postmating investment with an increasing risk and intensity of sperm competition may also drive the negative association between these investments across all 30 species. Such a negative relationship between pre-and postmating investment across species has been reported in several recent comparative studies (Poulin and Morand 2000;Fitzpatrick et al 2012;Lüpold et al 2014;Dines et al 2015;Kahrl et al 2016). In a broad intertaxonomic comparison of the interspecific relationship between these investments, negative trends have been found in those taxa in which most species show low levels of polyandry, whereas other taxa tend to exhibit a positive relationship ).…”

Sexual coloration and sperm performance in the Australian painted dragon lizard, Ctenophorus pictus

“…() suggested, based on theoretical analyses, that the degree to which males are able to monopolize access to females via precopulatory sexual selection (sensu Emlen & Oring, ) may determine the strength and direction of this trade‐off among species. Taxonomic comparisons support this argument, demonstrating that taxa in which males are able to monopolize females are more likely to exhibit a trade‐off between precopulatory armaments and testis size (Fitzpatrick et al ., ; Lupold et al ., ; Dines et al ., ; Dunn et al ., ; Kahrl et al ., ). Sperm performance has received minimal investigation as an important post‐copulatory trait in this framework (Locatello et al ., ; Pitcher et al ., ; Helfenstein et al ., ; Rowe et al ., ).…”

Sexual ornaments but not weapons trade off against testes size in primates

“…view. Comparative analyses have reported negative associations between testes size and male-biased sexual size dimorphism (SSD), and/or the exaggeration of weapons in taxa as diverse as parasitic worms [13], lizards and snakes [14], frogs [15], cetaceans [16] and pinnipeds [17]. Moreover, the strength of this association appears to reflect the degree to which pre-mating contest competition allows males to monopolize access to females [18].…”