Sexual Signal Evolution Outpaces Ecological Divergence during Electric Fish Species Radiation

Abstract

Natural selection arising from resource competition and environmental heterogeneity can drive adaptive radiation. Ecological opportunity facilitates this process, resulting in rapid divergence of ecological traits in many celebrated radiations. In other cases, sexual selection is thought to fuel divergence in mating signals ahead of ecological divergence. Comparing divergence rates between naturally and sexually selected traits can offer insights into processes underlying species radiations, but to date such comparisons have been largely qualitative. Here, we quantitatively compare divergence rates for four traits in African mormyrid fishes, which use an electrical communication system with few extrinsic constraints on divergence. We demonstrate rapid signal evolution in the Paramormyrops species flock compared to divergence in morphology, size, and trophic ecology. This disparity in the tempo of trait evolution suggests that sexual selection is an important early driver of species radiation in these mormyrids. We also found slight divergence in ecological traits among closely related species, consistent with a supporting role for natural selection in Paramormyrops diversification. Our results highlight the potential for sexual selection to drive explosive signal divergence when innovations in communication open new opportunities in signal space, suggesting that opportunity can catalyze species radiations through sexual selection, as well as natural selection.

Sensory receptor diversity establishes a peripheral population code for stimulus duration at low intensities

“…Thus, long-pass filtering in the KO electrosensory system establishes a basic mechanism for distinguishing behaviorally relevant variation in conspecific EOD duration. However, there is extensive overlap in EOD duration among sympatric species (Arnegard et al, 2010;Carlson et al, 2011;Hopkins, 1981), suggesting the need to precisely distinguish small differences in duration. Further, EODs are individually distinctive (Friedman and Hopkins, 1996), and there is evidence that some species of mormyrids can use this information to discriminate between individuals (Graff and Kramer, 1992).…”

How an ancient genome duplication electrified modern fish

“…Two unrelated lineages of fish, the mormyroids of Africa and the gymnotiforms of South America, have evolved similar electric organs and use them to produce signals used in courtship and territoriality (3). Within each species, males and females produce recognizably different signals, and sexual selection seems to play a major role in the diversification of signal types (2).…”

Genetic drift does not sufficiently explain patterns of electric signal variation among populations of the mormyrid electric fishParamormyrops kingsleyae

“…Arnegard et al (2010b) recently demonstrated that the evolution of electric signals far outpaces divergence in morphology, size and trophic ecology, implying over broad taxonomic scales, Paramormyrops diversification may largely have been driven by evolution of electric signals, however the source of variation upon which selection acts is presently unknown. Carlson et al (2011) suggests over broad taxonomic scales brain evolution in regions encoding temporal differences in EODs precedes EOD diversification.…”

“…Disruption of the behavioral coupling between signaler and receiver can increase the probability of reproductive isolation, and eventually speciation (Pillay and Rymer 2012), as evidenced by numerous rapidly evolved groups of species with highly diverse courtship signals (Diamond 1986;Allender et al 2003;Mendelson and Shaw 2005;Boul et al 2006;Mullen et al 2007;Arnegard et al 2010b). Several models of speciation strongly implicate the evolution of divergent mate choice behavior (or prezygotic mechanisms in general) in the speciation process (Lande 1981;Boughman 2002;Schluter 2009;van Doorn et al 2009), though it is presently a challenge in speciation research to disentangle the roles of natural selection, sexual selection, and drift in the early evolution of reproductive isolation (Butlin et al 2012).…”