Multiple host species maintain genetic diversity in herbivore populations

Abstract

How natural populations maintain genetic variation for fitness remains a central problem in evolutionary biology. Theory predicts that opposing selective pressures across environments can preserve fitness-associated polymorphism, but how interactions among species contribute to this process remains poorly understood. Here we show that host diversity preserves standing genetic variation within sexual populations of the leafmining fly Scaptomyza flava. We evolved twelve populations for ten generations on either of two naturally co-occurring host plants or on both, pooling survivors from the two hosts before mating. Single-host populations evolved reciprocal fitness trade-offs, whereas two-host populations maintained relatively even performance across hosts. Whole-genome time series dynamics identified a linked region in which alleles increased on one host and decreased on the other, while showing little net change under two-host conditions. Wild flies reared from the two hosts showed corresponding allele-frequency differences within this region. Across the genome, two-host populations retained more rare variants than populations evolving on either host alone. These findings show that selection imposed by different host species in sympatry can maintain standing genetic diversity within an herbivore population.