Multivariate divergence in wild microbes: no evidence for evolution along a genetic line of least resistance

Trait evolution depends both on the direct fitness effects of specific traits and on indirect selection arising from genetically correlated traits. Although well established in plants and animals, the role of trait correlations in microbial evolution remains a major open question. Here, we tested whether genetic correlations in a suite of metabolic traits are conserved between two sister lineages of fungal endophytes, and whether phenotypic divergence between lineages occurred in the direction of the multivariate trait combination containing the most genetic variance within lineages i.e., the genetic lines of least resistance. We found that while one lineage grew faster across nearly all substrates, lineages differed in their mean response to specific substrates and in their overall multivariate metabolic trait means. The structure of the genetic variance-covariance (G) matrix was conserved between lineages, yet to our surprise, divergence in metabolic phenotypes between lineages was nearly orthogonal to the major axis of genetic variation within lineages, indicating that divergence did not occur along the genetic lines of least resistance. Our findings suggest that the evolutionary genetics of trait correlations in microorganisms warrant further research, and highlight the extensive functional variation that exists at very fine taxonomic scales in host-associated microbial communities.