Adaptive introgression from distant Caribbean islands contributed to the diversification of a microendemic adaptive radiation of trophic specialist pupfishes

Abstract

Rapid diversification often involves complex histories of gene flow that leave variable and conflicting signatures of evolutionary relatedness across the genome. Identifying the extent and source of variation in these evolutionary relationships can provide insight into the evolutionary mechanisms involved in rapid radiations. Here we compare the discordant evolutionary relationships associated with species phenotypes across 42 whole genomes from a sympatric adaptive radiation of Cyprinodon pupfishes endemic to San Salvador Island, Bahamas and several outgroup pupfish species in order to understand the rarity of these trophic specialists within the larger radiation of Cyprinodon. 82% of the genome depicts close evolutionary relationships among the San Salvador Island species reflecting their geographic proximity, but the vast majority of variants fixed between specialist species lie in regions with discordant topologies. Top candidate adaptive introgression regions include signatures of selective sweeps and adaptive introgression of genetic variation from a single population in the northwestern Bahamas into each of the specialist species. Hard selective sweeps of genetic variation on San Salvador Island contributed 5 times more to speciation of trophic specialists than adaptive introgression of Caribbean genetic variation; however, four of the 11 introgressed regions came from a single distant island and were associated with the primary axis of oral jaw divergence within the radiation. For example, standing variation in a proto-oncogene (ski) known to have effects on jaw size introgressed into one San Salvador Island specialist from an island 300 km away approximately 10 kya. The complex emerging picture of the origins of adaptive radiation on San Salvador Island indicates that multiple sources of genetic variation contributed to the adaptive phenotypes of novel trophic specialists on the island. Our findings suggest that a suite of factors, including rare adaptive introgression, may be necessary for adaptive radiation in addition to ecological opportunity.

Don't throw out the sympatric speciation with the crater lake water: fine-scale investigation of introgression provides equivocal support for causal role of secondary gene flow in one of the clearest examples of sympatric speciation

“…; Meier et al. ), including our own previous work (Richards and Martin ). For example, several studies have found convincing candidate genes/variants in introgressed regions suggesting that adaptive introgression played a role in shaping ecological and morphological diversity.…”

“…These include the detection of introgressed alleles linked to wing‐color patterning involved in mimicry and mate selection in Heliconius butterflies (The Heliconius Genome Consortium et al. ), flower coloration involved in pollinator preferences for Mimulus species (Stankowski and Streisfeld ), and oral jaw size variation involved in scale‐eating trophic specialization in Cyprinodon pupfishes (Richards and Martin ).…”

Speciation in sympatry with ongoing secondary gene flow and a potential olfactory trigger in a radiation of Cameroon cichlids

“…For instance, secondary colonization may involve a partially reproductively isolated population, in which case any resulting speciation event would have had a crucial allopatric phase. Second, the introduction of novel genetic variation and novel allelic combinations may promote speciation more generally, for example, via the formation of a hybrid swarm (Kautt, Machado‐Schiaffino, Meyer et al., ; Meier, Marques, Wagner, Excoffier, & Seehausen, ; Meier et al., ; Seehausen, ), transgressive segregation (Kagawa & Takimoto, ), or adaptive introgression (Anderson, ; Feder et al., ; Heliconius Genome Consortium, ; Pardo‐Diaz et al., ; Richards & Martin, ; Stankowski & Streisfeld, ).…”

“…A role for secondary gene flow would be supported if divergence rapidly followed a discrete admixture event (Kautt, Machado‐Schiaffino, Meyer et al., ); whereas if gene flow took place only after the onset of divergence, such a role would seem unlikely. Genomic data can also be used to identify segments of the genome that have experienced admixture and to examine whether these contain genes that may have been important in speciation (Lamichhaney et al., ; Meier et al., ; Richards & Martin, ).…”

An embryonic staging series up to hatching for Cyprinodon variegatus: An emerging fish model for developmental, evolutionary, and ecological research

“…Research on Cyprinodon spans an array of disciplines including phylogenetic inferences of North American paleoenvironments (Echelle, ; Echelle et al, ) use as models to understand how organisms adapt and tolerate stressful environments (Naiman, Gerking, & Ratcliff, ; Naiman, Gerking, & Stuart, ; Plath & Strecker, ), as ecotoxicology models and biological indicators of estuarine health (Bowman, Kroll, Hemmer, Folmar, & Denslow, ; Raimondo et al, ), and as conservation models to understand the dynamics of small population size (Martin et al, ; Sağlam et al, ). Furthermore, evolutionary biologists study fishes in the genus Cyprinodon to understand the mating behavior (Kodric‐Brown, ; West & Kodric‐Brown, ), speciation and hybridization (Martin, ; Martin & Feinstein, ; McGirr & Martin, ; Richards & Martin, ; Rosenfield & Brown, ; Turner, Duvernell, Bunt, & Barton, ), and the role of developmental plasticity in morphological evolution (Lema, , , ). Our own research is developing Cyprinodon as an evolutionary developmental model to understand the genetic sources of skull morphological variation (Lencer et al, , ).…”