The cryptic origins of evolutionary novelty: 1,000-fold-faster trophic diversification rates without increased ecological opportunity or hybrid swarm

Abstract

Ecological opportunity is frequently proposed as the sole ingredient for adaptive radiation into novel niches. Alternatively, genome-wide hybridization resulting from hybrid swarm may be the trigger. However, these hypotheses have been difficult to test due to the rarity of comparable control environments lacking adaptive radiations. Here I exploit such a pattern in microendemic radiations of Caribbean pupfishes. I show that a sympatric three-species radiation on San Salvador Island, Bahamas diversified 1,445 times faster than neighboring islands in jaw length due to evolution of a novel scale-eating adaptive zone from a generalist ancestral niche. I then sampled 22 generalist populations on seven neighboring islands and measured morphological diversity, stomach content diversity, dietary isotopic diversity, genetic diversity, lake/island areas, macroalgae richness, and Caribbean-wide patterns of gene flow. None of these standard metrics of ecological opportunity or gene flow were associated with adaptive radiation, except for slight increases in macroalgae richness. Thus, exceptional trophic diversification is highly localized despite myriad generalist populations in comparable environmental and genetic backgrounds. This study provides a strong counterexample to the ecological/hybrid-swarm theories of adaptive radiation and suggests that diversification of novel specialists on a sparse fitness landscape is constrained by more than ecological opportunity and gene flow.