The paradox behind the pattern of rapid adaptive radiation: how can the speciation process sustain itself through an early burst?

Abstract

Rapid adaptive radiation poses a distinct question apart from speciation and adaptation: what happens after one speciation event? That is, how are some lineages able to continue speciating through a rapid burst? This question connects global macroevolutionary patterns to microevolutionary processes. Here we review major features of rapid radiations in nature and their mismatch with theoretical models and what is currently known about speciation mechanisms. Rapid radiations occur on three major diversification axes - species richness, phenotypic disparity, and ecological diversity - with exceptional outliers on each axis. The paradox is that the hallmark early stage of adaptive radiation, a rapid burst of speciation and niche diversification, is contradicted by most existing speciation models which instead predict continuously decelerating speciation rates and niche subdivision through time. Furthermore, while speciation mechanisms such as magic traits, phenotype matching, and physical linkage of co-adapted alleles promote speciation, it is often not discussed how these mechanisms could promote multiple speciation events in rapid succession. Additional mechanisms beyond ecological opportunity are needed to understand how rapid radiations occur. We review the evidence for five emerging theories: 1) the 'transporter' hypothesis: introgression and the ancient origins of adaptive alleles, 2) the 'signal complexity' hypothesis: the dimensionality of sexual traits, 3) the connectivity of fitness landscapes, 4) 'diversity begets diversity', and 5) flexible stem/'plasticity first'. We propose new questions and predictions to guide future work on the mechanisms underlying the rare origins of rapid radiation.