Mosaic evolution of grasping and genitalic traits in two sympatric scorpion species with reproductive interference

Abstract

Reproductive interference (RI) can occur when two related species coexist in sympatry, involving sexual attraction, mating, and even hybridization between heterospecifics. Consequently, reproductive key characters of these species may suffer morphological shifts in sympatry to avoid the success of heterospecific sexual interactions, a phenomenon known as reproductive character displacement (RCD). RCD can be promoted by natural selection, although sexual selection pressures can act synergistically or agonistically so that phenotypic variation can respond in different directions and magnitudes to these forces. In turn, the size and shape of characters may respond differentially (mosaic evolution) to these pressures, so the analysis of multiple dimensions in traits is essential to understand the complexity of their phenotypic variability. To date, there are no studies evaluating this topic in scorpions, and two species (Urophonius brachycentrus and U. achalensis) sympatric and synchronous with RI represent an ideal model to evaluate the phenotypic variation and occurrence of RCD. In addition, the populations of these species are found in an altitudinal cline, so environmental factors may also be responsible for explaining their morphological variation. We compared the intra-specific variation, the size and shape of multiple characters involved in courtship, and sperm transfer in individuals from sympatric and allopatric populations using geometric morphometrics. We found asymmetric RCD of several sexual characters for courtship success (grasping structures) and sperm transfer (genital characters). This would evidence the action of natural selection pressures and the existence of a possible mechanism to avoid heterospecific mating success. In addition, we found a pattern of asymmetric morphological variation where one species in the sympatric zone suffered an increase in size in several characters due to environmental factors (pattern of morphological convergence). The convergence of characters combined with RI and a scramble competition mating system could intensify sexual selection pressures on specific characters, which was reflected in their high coefficients of variation. Our results suggest that in this sympatric zone, several selective regimes act differentially on various dimensions of the characters evaluated, which would support a possible mosaic evolution. This comprehensive study illuminates the complexity inherent in the evolution of multi-functional traits in a previously unexplored model, providing novel insights for evaluating traits under multiple selective pressures in animal systems experimenting RI.