Sexual Dichromatism Drives Diversification within a Major Radiation of African Amphibians

Abstract

Theory predicts that sexually dimorphic traits under strong sexual selection, particularly those involved with intersexual signaling, can accelerate speciation and produce bursts of diversification. Sexual dichromatism (sexual dimorphism in color) is widely used as a proxy for sexual selection and is associated with rapid diversification in several animal groups, yet studies using phylogenetic comparative methods to explicitly test for an association between sexual dichromatism and diversification have produced conflicting results. Sexual dichromatism is rare in frogs, but it is both striking and prevalent in African reed frogs, a major component of the diverse frog radiation termed Afrobatrachia. In contrast to most other vertebrates, reed frogs display female-biased dichromatism in which females undergo color transformation, often resulting in more ornate coloration in females than in males. We produce a robust phylogeny of Afrobatrachia to investigate the evolutionary origins of sexual dichromatism in this radiation and examine whether the presence of dichromatism is associated with increased rates of net diversification. We find that sexual dichromatism evolved once within hyperoliids and was followed by numerous independent reversals to monochromatism. We detect significant diversification rate heterogeneity in Afrobatrachia and find that sexually dichromatic lineages have double the average net diversification rate of monochromatic lineages. By conducting trait simulations on our empirical phylogeny, we demonstrate that our inference of trait-dependent diversification is robust. Although sexual dichromatism in hyperoliid frogs is linked to their rapid diversification and supports macroevolutionary predictions of speciation by sexual selection, the function of dichromatism in reed frogs remains unclear. We propose that reed frogs are a compelling system for studying the roles of natural and sexual selection on the evolution of sexual dichromatism across micro- and macroevolutionary timescales.

Congolius, a new genus of African reed frog endemic to the central Congo: A potential case of convergent evolution

“…African reed frogs, Hyperoliidae Laurent, 1943, are presently encompassing almost 230 species in 17 genera. These are split into two subfamilies, Hyperoliinae Laurent, 1943 with 12 genera, and the less speciose subfamily Kassininae Laurent, 1972 with 5 genera 1 , 2 (Table 1 ). The phylogenetic relationships among the hyperoliid frogs are still not completely understood, and the systematics has undergone recent changes, e.g., revalidation of the subfamily Kassininae and reclassification of Acanthixalus to this subfamily 1 or genus-level reorganizations in some species 3 .…”

“…These are split into two subfamilies, Hyperoliinae Laurent, 1943 with 12 genera, and the less speciose subfamily Kassininae Laurent, 1972 with 5 genera 1 , 2 (Table 1 ). The phylogenetic relationships among the hyperoliid frogs are still not completely understood, and the systematics has undergone recent changes, e.g., revalidation of the subfamily Kassininae and reclassification of Acanthixalus to this subfamily 1 or genus-level reorganizations in some species 3 . There is also a number of genera whose classification to the family is clear on the basis of morphological characters, but their exact phylogenetic position is still an unanswered question.…”

“…Some previous morphological studies provided rough ideas where these genera might be phylogenetically placed 8 , 9 , but the first two genera have never been studied by a molecular approach. All three genera are presently placed in Hyperoliinae 1 , 2 , neverthless, the hypothesized sister relationship of Callixalus and Acanthixalus 8 , 9 keeps the question on the phylogenetic position of Callixalus open. Similar uncertainties apply to Chrysobatrachus and Kassinula .…”

“…The study included phylogenetic analysis of three mitochondrial markers, which did place the genus in Hyperoliidae, but did not resolve its exact systematic position. Later studies, which comprised phylogenetic or phylogenomic analyses of nuclear DNA, uncovered affiliation of Morerella to Cryptothylax from Central African rain forests 1 , 3 .…”

Correlated evolution of parental care with dichromatism, colour, and patterns in anurans

“…The adaptive significance of background matching by camouflage as well as aposematism to overcome predation is well supported at multiple scales [e.g., 36,39,[40][41][42][43][44]. Dichromatism, which has so far been observed in ~2% of extant anurans [45], is also an effective strategy to achieve crypticity, however the frequency of dichromatism is likely to be an underestimate, owing to the ephemeral nature of dynamic dichromatism [22] and the general lack of studies on anurans [21,22]. Although evidence of the adaptive value of colours and patterns in shaping life-history traits is emerging, none, to the best of our knowledge, examine if costly life-history traits such as parental care are associated with dichromatism as well as specific dorsal colours, and patterns.…”