Behavioral and phenotypic constraint belie deep genomic divergence and seasonal adaptation in a widespread desert lizard

Abstract

Cryptic species offer opportunities to reveal the mechanisms that constrain phenotypic divergence during speciation. We integrated whole-genome sequencing, morphological, micro- and macro-climatic, and behavioral data to investigate divergence across a well- documented genetic break in the desert-adapted side-blotched lizard, Uta stansburiana, on the Baja California peninsula. Despite deep genomic differentiation, clades show remarkable similarity in morphology, habitat use, and thermal biology. Nearly all genetic differentiation (87%) is explained by isolation by distance and seasonal variation in precipitation, with almost no effect of temperature. Behavioral thermoregulation and changes in activity time accommodate strong macro- and micro-climatic differences, buffering against selection that would otherwise drive morphological and physiological divergence. In contrast, genomic signatures of selection and divergence in genes associated with the nervous system, sensory perception, and biomolecule metabolism indicate adaptation to differences in rainfall seasonality. The results show behavioral flexibility can constrain phenotypic divergence, yielding cryptic species-level genetic divergence despite strong eco-climatic disparities and selection pressures. More broadly, this study shows how rigorous statistical integration of multiple data types can disentangle competing eco- climatic drivers that can decouple phenotype from genotype during speciation. SignificanceUnderstanding why deep genetic divergence occurs without phenotypic differentiation is a longstanding challenge in evolutionary biology. By statistically integrating genomic, morphological, climatic, and behavioral data, we test the mechanisms controlling differentiation within a natural lizard system in a geo-climatically diverse setting. Results show that isolation by distance and adaptation to precipitation seasonality drive nearly all genomic differentiation. Behavioral adjustment to strong thermal variation buffers against selection pressure otherwise expected to cause divergence in morphology, thermal biology, and habitat use. This work demonstrates how rigorous integrative analyses can tease apart ecological and neutral factors controlling genomic divergence, providing rare insight into causal mechanisms driving speciation while constraining phenotypic divergence.