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.

Keywords: Phylogenetic comparative method; sexual size dimorphism; sperm competition; testis size.

Figure 1

Partial slopes (±SE) from phylogenetic generalized least squares (PGLS, black) and ordinary least squares (OLS, white) regressions of log₁₀ testis size on log₁₀ sexual size dimorphism (SSD) with log₁₀ snout‐vent length (SVL) as a covariate. We conducted separate regressions for all lineages represented by ≥8 species, with sample sizes for each lineage shown at the tips of the phylogeny.

Figure 2

(A, B) Relationships between phylogenetically adjusted and size‐corrected measures of testis size and sexual size dimorphism (SSD) across (A) 120 lizard species and (B) 31 snake species. Residuals were obtained from phylogenetic generalized least squares (PGLS) regression of log₁₀ testis size on log₁₀ SVL (residual testis size) and PGLS regression of log₁₀ SSD on log₁₀ SVL (residual SSD). These residuals were used to visualize the covariance between testis size and SSD after accounting for phylogeny and allometry, but actual inferences (and reported partial r‐ and P‐values) are based on multiple regressions using PGLS with a size covariate. (C, D) Relationships between size‐corrected residuals obtained from regression (through the origin) of phylogenetically independent contrasts for log₁₀ SSD regressed on independent contrasts for log₁₀ SVL (residual contrasts of SSD) and of independent contrasts for log₁₀ testis size regressed on independent contrasts for log₁₀ SVL (residual contrasts of testis size). As above, relationships are shown separately for (C) lizards (N = 119 contrasts) and (D) snakes (N = 30 contrasts).