Genome-wide signatures of reproductive isolation shape the varied genomic landscape of the roundtail horned lizard (Phrynosoma modestum)

Abstract

Population divergence is promoted and inhibited by gene flow and divergent selection, but the mechanisms of and relationship between these two processes remain poorly understood. Modelling the selective pressures at play in a natural population requires a thorough understanding of species structure and demographic history, which can be helpful in hypothesizing the genetic and evolutionary factors that underlie divergence. In this study, we assess whole genome sequences of round-tailed horned lizards (Phyrnosoma modestum) from throughout the species range and combine phylogenetic analyses with genetic landscape scans to understand how current genetic diversity has been influenced by demographic histories and evolutionary pressures. Maximum likelihood phylogenetic analysis supports two lineages within the species, correlating with a North/South population divide that likely diverged about 7 Ma and displayed little migration. Intermediate gdi values indicate that the two lineages may be in the gray area of speciation, yet our results also support significant isolation-by-distance (IBD). Negative values of Tajimas D offer support for selection acting on P. modestum, but may stem from recent population expansions. Genomic diversity within populations and islands of divergence between populations are also detected across the P. modestum genome, specifically exhibiting differentiation patterns linked to reproductive isolation and within-population selection. We posit potential explanations for the genomic landscape characterized here, namely that allopatry plays a large role in shaping genomic divergence across the species range. Taken together, our results provide a picture of a species currently maintaining species integrity despite significant genomic signatures of geographic structure and reproductive isolation.