Hybridization masks speciation in the evolutionary history of the Galápagos marine iguana

Abstract

The effects of the direct interaction between hybridization and speciation-two major contrasting evolutionary processes-are poorly understood. We present here the evolutionary history of the Galápagos marine iguana (Amblyrhynchus cristatus) and reveal a case of incipient within-island speciation, which is paralleled by between-island hybridization. In-depth genome-wide analyses suggest that Amblyrhynchus diverged from its sister group, the Galápagos land iguanas, around 4.5 million years ago (Ma), but divergence among extant populations is exceedingly young (less than 50 000 years). Despite Amblyrhynchus appearing as a single long-branch species phylogenetically, we find strong population structure between islands, and one case of incipient speciation of sister lineages within the same island-ostensibly initiated by volcanic events. Hybridization between both lineages is exceedingly rare, yet frequent hybridization with migrants from nearby islands is evident. The contemporary snapshot provided by highly variable markers indicates that speciation events may have occurred throughout the evolutionary history of marine iguanas, though these events are not visible in the deeper phylogenetic trees. We hypothesize that the observed interplay of speciation and hybridization might be a mechanism by which local adaptations, generated by incipient speciation, can be absorbed into a common gene pool, thereby enhancing the evolutionary potential of the species as a whole.

Gecko phylogeography in the Western Indian Ocean region: the oldest clade of Ebenavia inunguis lives on the youngest island

“…More recent studies have provided younger estimates for some of the taxa involved (e.g. MacLeod et al ., , for Galápagos iguanas).…”

Emergence/Subsidence Histories Along the Carnegie and Cocos Ridges and Their Bearing Upon Biological Speciation in the Galápagos

“…These distances and timescales should be taken into account by evolutionary biologists studying speciation events along the Galápagos/Carnegie/Cocos Ridge system, especially if South American origins are being considered, which is the case for most of the Galápagos endemic land faunal species (e.g., Parent et al, ). Our findings, coming from physical and geological arguments, pose important constraints to the evolutionary‐biology assessments of divergence and speciation ages for the region, which suggest well‐determined times for events occurring in the last 5 Ma (e.g., MacLeod et al, ), but open interval times for events before ~10 Ma (Parent et al, ), or highly uncertain yet crucial times for primary iguana‐ancestors divergence events for example at 35 ± 8 Ma (MacLeod et al, ), and should be ultimately contextualized in deep‐time assessments of the iguanian lizard phylogeny such as that presented by Townsend et al (), with important divergence events for Pleurodonta at about ~70 Ma and Acrodonta at ~90 Ma (both with confidence‐interval radii of about 10 Ma, and suggesting origin locations in North and Central Americas, with later migration to South America). Although the corresponding uncertainties are naturally large, there is hope that future technological advances will allow precision refinement both in biology and geology.…”

Hybridizing salamanders experience accelerated diversification

“…Although 459 other factors certainly contribute to the observed diversification dynamics, we have shown that 460 hybridization plays a significant role, while accounting for hidden, correlated states in our 461 analysis. Nearly all studies of hybridization have focused on individual case studies in which 462 hybridization results in species collapse 66 or promotes diversification in a single species 463 group 12,13,20,25 . Such studies are necessarily limited in the extent to which their results may be 464 generalized 28 , particularly because results were equivocal across studies.…”

“…44 Interest in hybrid-mediated speciation has recently burgeoned, but studies have typically 45 been limited in taxonomic scope. Studies of the effect of hybridization on diversification have 46 most commonly been conducted among closely related pairs or small clades of taxa, and results 47 have been equivocal 1, 20,21,22,23,24,25,26 . Additionally, studies of hybridization often occur along 48 different stages of the speciation continuum 27 , whereby hybridization can appear as a force that 49 either facilitates or impedes speciation.…”