Dimensionality of mate choice, sexual isolation, and speciation

Abstract

Multiple cues, across multiple sensory modalities, are involved in mate choice in a wide range of animal taxa. This multiplicity leads to the prediction that, in adaptive radiations, sexual isolation results from divergence in multiple dimensions. However, difficulties in directly measuring preferences and detecting multiple effects limit our ability to empirically assess the number of independent traits contributing to mate choice and sexual isolation. We present an approach to estimate the dimensionality of sexual isolation using mating trials across groups of related populations. We analyze nine radiations: seven in fruit flies (Drosophila) and one each in salamanders (Desmognathus) and cichlid fishes (Pseudotropheus). We find strong evidence that multiple latent traits--linear combinations of phenotypic traits and preferences--are responsible for the patterns of sexual isolation in all nine radiations but that dimensionality has a strong upper limit. Just two latent traits are implicated in the majority of cases. Mapping along latent trait axes tests predictions of sexual-selection models and allows correlation with specific phenotypic traits and functional components of mate choice. We find support for the role of stabilizing natural selection on the sexually selected (male) traits. In the cichlids, latent-trait axes incorporate male-coloration patterns and exhibit convergence as well as divergence among populations. In the salamanders, temporal patterning in sensory modalities and male vs. female preferences are reflected in different latent-trait axes.

Fig. 1.

Schematic diagram of the mate-choice model for two populations (A and B) in two latent-trait dimensions, with population means (solid circles) and within-population variation (dashed circles) for male traits (blue; z) and female preferences (red; y). The probability of mating between, for example, a female chosen randomly from population B (star 1) and a male chosen from either the same population (star 2) or population A (star 3) is a function of the distance between them (black dotted lines) in this phenotypic space.

Fig. 2.

Best-fit male (blue) and female (red) population means for latent traits underlying sexual isolation in nine radiations. Black lines link male and female means for each population. For all but A and G, these two axes represent the best-fit number of dimensions; for A and G, these are the first two of three or four axes, respectively. Canonical correlation-redundancy indices (bottom right of each plot) show the proportion of female variance explained by males of the same population (red) and male variance explained by females (blue). (A) Desmognathus (24); dashed lines enclose populations in three currently recognized species. (B) D. paulistorum, Amazonian race (26). (C) D. paulistorum, Andean–South Brazilian race (26). (D) D. paulistorum, multiple races (26). (E) D. sturtevanti (27). (F) D. willistoni (28). (G) D. prosaltans (29). (H) D. auraria complex (31). (I) Pseudotropheus (30); labels indicate populations.