Local adaptation does not lead to genome-wide differentiation in lava flow lizards

Adaptation can occur with or without genome-wide differentiation. If adaptive loci are linked to traits involved in reproductive isolation, genome-wide divergence is likely, and speciation is possible. However, adaptation can also lead to phenotypic differentiation without genome-wide divergence if levels of ongoing gene flow are high. Here, we use the replicated occurrence of melanism in lava flow lizards to assess the relationship between local adaptation and genome-wide differentiation. We compare patterns of phenotypic and genomic divergence among lava flow and nonlava populations for three lizard species and three lava flows in the Chihuahuan Desert. We find that local phenotypic adaptation (melanism) is not typically accompanied by genome-wide differentiation. Specifically, lava populations do not generally exhibit greater divergence from nonlava populations than expected by geography alone, regardless of whether the lava formation is 5,000 or 760,000 years old. We also infer that gene flow between lava and nonlava populations is ongoing in all lava populations surveyed. Recent work in the isolation by environment and ecological speciation literature suggests that environmentally driven genome-wide differentiation is common in nature. However, local adaptation may often simply be local adaptation rather than an early stage of ecological speciation.