We get by with a little help from our friends: shared adaptive variation provides a bridge to novel ecological specialists during adaptive radiation

Abstract

Adaptive radiations involve astounding bursts of phenotypic, ecological, and species diversity. However, the microevolutionary processes that underlie the origins of these bursts are still poorly understood. We report the discovery of a cryptic intermediate wide-mouth scale-eating ecomorph in a recent radiation of Cyprinodon pupfishes which provides crucial information about the evolutionary and ecological transition from a widespread algae-eating generalist to a novel microendemic scale-eating specialist. We first show that this ecomorph occurs in sympatry with generalist C. variegatus and scale-eating specialist C. desquamator across several hypersaline lakes on San Salvador Island, Bahamas, but is genetically differentiated, morphologically distinct when reared in a common garden, and sometimes consumes scales. We then compared the timing of selective sweeps on shared and unique adaptive variants in both scale-eating species to characterize the evolutionary path to scale-eating. We predicted that adaptation to the intermediate wide-mouth scale-eating niche aided in the rapid divergence of the more specialized scale-eater C. desquamator. Therefore, selection for shared adaptive variants would occur first in wide-mouth. Contrary to our prediction, four of the six sets of shared adaptive alleles in both scale-eating species swept significantly earlier in C. desquamator. Adaptive introgression from the specialist into the wide-mouth ancestor may have resulted in parallel evolution of their dietary niche. Conversely, no adaptive alleles for scale-eating were reused in a third sympatric specialist C. brontotheriodes, despite sharing 9% of hard selective sweeps. Our work provides a microevolutionary framework for investigating how diversity begets diversity during adaptive radiation.

Trophic Specialization on unique resources despite limited niche divergence in a celebrated example of sympatric speciation

“…Adaptive radiations are a hallmark of evolutionary biology, being among the most celebrated, studied and charismatic examples of ecological diversity. Much research on these systems centres on uncovering the mechanisms driving diversification (Martin & Richards, 2019; Schluter, 2000; Stroud & Losos, 2020), and there are several hypotheses suggesting that specific temporal, spatial, environmental and/or genomic factors are necessary for a radiation to proceed (Schluter, 2000; Gavrilets & Losos, 2009; Richards & Martin, 2021). Many of these theories highlight the importance of divergence in trophic niche, as dietary niche partitioning can allow for the coexistence of similar species by reducing interspecific competition for limited food resources (Correa & Winemiller, 2014; Reinthal, 1990; Ross, 1986; Varghese et al, 2014; Winemiller & Pianka, 1990).…”