Elevated genetic load is associated with reduced bite force in insular lizard populations

Abstract

Demographic history can profoundly shape genomic variation by altering levels of inbreeding, the strength of genetic drift, and the efficacy of purifying selection, thereby influencing both the accumulation and expression of deleterious variation. Yet the extent to which these genomic consequences translate into organismal performance remains poorly understood. Here, we investigated how contrasting demographic histories shape genomic diversity, inbreeding, genetic load, and performance across mainland and insular populations of the Italian wall lizard, Podarcis siculus. Using whole-genome sequence data from 263 wild-caught individuals and field-based performance measurements from 134 lizards, we characterised population structure and demographic history, quantified genomic diversity, runs of homozygosity, and deleterious variation, and tested associations between genomic inbreeding and performance traits. Island populations showed reduced genetic diversity, increased autozygosity, and elevated genetic load relative to mainland populations, consistent with stronger genetic drift and reduced efficacy of purifying selection. Patterns of deleterious variation were consistent with purging of strongly, but not mildly, deleterious variants. Greater genomic autozygosity was associated with reduced bite force in island lizards, a pattern consistent with inbreeding depression, whereas sprint speed, sperm quality, immunocompetence, and spatial cognition showed no significant association with inbreeding. Genome-wide mapping of runs of homozygosity further identified multiple genomic regions associated with reduced bite performance. Together, these results show how demographic history shapes genomic diversity, homozygosity, and deleterious variation in wild vertebrate populations, while revealing that phenotypic consequences can be trait-specific, a pattern that may reflect differences in genetic architecture and the extent of environmental influence on trait variation.