A few genes modulate the ecological impact of a freshwater fish species on food webs and ecosystem functions

Abstract

Genetic diversity within species can shape food webs and ecosystem functioning as strongly as species diversity, yet the genomic architecture underlying these effects remains unclear. Gene-to-ecosystem relationships may arise from genome-wide diversity, from a limited number of ecologically-important genes, or a combination of both. Experimental tests of these hypotheses are lacking. Here, we manipulated genomic diversity of a top-predatory fish in mesocosms under ambient or warm conditions, and quantified ecological responses spanning fish biomass, prey communities and ecosystem functions. Genome-wide diversity explained few ecological responses, with moderate effects (r=0.260). In contrast, variation at specific candidate SNPs predicted all ecological responses consistently across climatic conditions, with effect sizes being more than twice those of genome-wide estimates (r=0.599). Moreover, combining information from small subsets of candidate SNPs outperformed both single-locus and genome-wide diversity for all ecological responses (r=0.841), consistent with an oligogenic architecture for gene-to-ecosystem relationships. Enrichment analyses revealed functional pathways related to growth, development and metabolic regulation, driven by a small set of pleiotropic genes. We demonstrate that the ecological consequences of intraspecific genetic variation arose from a limited fraction of the genome, highlighting the importance of functional genomic structure, rather than genome-wide diversity alone, in shaping eco-evolutionary dynamics.