Lichen symbiosis does not impose a uniform genomic syndrome on algae

Abstract

Symbiosis has lasting effects on the genomic evolution of interacting organisms. Shifting niches and selection intensities are well-documented drivers of adaptive evolution, but nonadaptive evolution is an equally important, if less conspicuous, dimension of symbiont genome evolution. Through a reduction in effective population size (Ne), symbiosis can reduce the efficacy of natural selection in symbionts; however, evidence of this "genomic syndrome" is derived almost entirely from bacteria. Whether it extends to eukaryotic symbioses with complex demography remains unclear. Here, lichen-forming algae are examined for signatures of a genome-wide reduction in the efficacy of selection arising from demographic shifts associated with symbiosis. To test this, four lichen-forming algal taxa were compared to their closest free-living relatives using complementary measures of (i) the strength of molecular evolution (dN/dS, K), (ii) codon use bias (ENC), and (iii) base composition at synonymous sites (GC3). Lichen-forming algae showed heterogeneous responses across all signatures of molecular evolution examined. The effect of lifestyle (lichen-forming vs. free-living) on dN/dS ratios and codon use bias was lineage specific. GC3 was uniformly reduced in lichen-forming taxa, but the underlying causes differed, and no genes showed uniformly intensified or relaxed selection across all four lichen-forming taxa. These results suggest that, while symbiosis often reshapes symbiont population genetics in ways that elevate the role of drift, lichen-forming algae do not show a uniform reduction in the efficacy of selection. Rather, the demographic effects and functional demands of each specific lichen symbiosis likely shape genome evolution in lineage-specific ways.