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 an intermediate C. sp. ‘wide-mouth’ scale-eating ecomorph in a sympatric radiation of Cyprinodon pupfishes, illuminating the 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 on San Salvador Island, Bahamas, but is genetically differentiated, morphologically distinct and often consumes scales. We then compared the timing of selective sweeps on shared and unique adaptive variants in trophic specialists to characterize their adaptive walk. Shared adaptive regions swept first in both the specialist desquamator and the intermediate ‘wide-mouth’ ecomorph, followed by unique sweeps of introgressed variation in ‘wide-mouth’ and de novo variation in desquamator . The two scale-eating populations additionally shared 9% of their hard selective sweeps with the molluscivore C. brontotheroides , despite no single common ancestor among specialists. Our work provides a new microevolutionary framework for investigating how major ecological transitions occur and illustrates how both shared and unique genetic variation can provide a bridge for multiple species to access novel ecological niches.

Multiple performance peaks for scale-biting in an adaptive radiation of pupfishes

“…sp. ‘broadmouth’ F1 hybrids from Osprey Lake (Richards and Martin, 2022). Prior to filming, pupfishes were fed exclusively Repashy Superfood gel diets for acclimation and training for at least one week before filming.…”

“…F1 hybrid and F2 hybrid intercrosses were generated from molluscivore x scale-eater crosses from both Osprey Lake and Crescent Pond, generalist x scaleeater and generalist x molluscivore crosses from Little Lake, and generalist x C. sp. 'broadmouth' F1 hybrids from Osprey Lake (Richards and Martin, 2022). Prior to filming, pupfishes were fed exclusively Repashy Superfood gel diets for acclimation and training for at least one week before filming.…”

“…In several interior hypersaline lakes on San Salvador Island (SSI), C. desquamator occurs in sympatry at low frequencies in the same benthic macroalgae-dominated habitats as C. variegatus , a widespread generalist species, C. brontotheroides , an endemic oral-shelling molluscivore species, and C. sp. ‘wide-mouth’, a newly discovered intermediate scale-eating ecomorph which is not included in this study (Hernandez et al, 2018; Martin and Feinstein, 2014; Richards and Martin, 2022; St John et al, 2020).…”

Jaw size variation is associated with a novel craniofacial function for galanin receptor 2 in an adaptive radiation of pupfishes

“…Here we demonstrate the utility of an evolutionary radiation of Cyprinodon pupfishes for discovering and validating the craniofacial function of a new gene associated with jaw evolution via QTL and GWAS analyses. Pupfishes offer some advantages over other evolutionary fish systems because they (1) rapidly evolved highly divergent and unique craniofacial phenotypes (figure 1) with minimal genetic differentiation among species [43][44][45][46][47][48][49][50], (2) speciated in the face of ongoing gene flow resulting in very few highly differentiated genomic regions associated with species-specific craniofacial traits [51][52][53][54][55][56][57], and (3) are highly amenable to laboratory rearing and imaging due to their high fecundity, daily egg production, and egg transparency comparable to zebrafish [58,59]. This radiation contains the widespread algae-eating generalist pupfish, Cyprinodon variegatus (figure 1a), which is broadly distributed across the Caribbean and North American Atlantic coast and occurs in sympatry with two microendemic trophic specialist species found only in the hypersaline lakes of San Salvador Island (SSI), Bahamas.…”

“…Previous genomic and transcriptomic work on the SSI pupfishes identified dozens of new candidate craniofacial genes never previously characterized as craniofacial or directly investigated in other systems [54,56,57,[62][63][64][65][66][67]. One of the most promising candidates was galanin receptor 2a, the second receptor type for the galanin peptide.…”