Transgressive hybrids as hopeful holobionts

Hybridization between evolutionary lineages has profound impacts on the fitness and ecology of hybrid progeny. In extreme cases, the effects of hybridization can transcend ecological timescales by introducing trait novelty upon which evolution can act. Indeed, hybridization can even have macroevolutionary consequences, for example, as a driver of adaptive radiations and evolutionary innovations. Accordingly, hybridization is now recognized as a motor for macrobial evolution. By contrast, there has been substantially less progress made towards understanding the positive eco-evolutionary consequences of hybridization on holobionts. Rather, the emerging paradigm in holobiont literature is that hybridization disrupts symbiosis between a host lineage and its microbiome, leaving hybrids at a fitness deficit. These conclusions, however, have been drawn based on

Transgressive segregation of HA microbiota traits is not only limited to hybrids at a fitness deficit but also occurs in ecologically successful hybrids. This suggests that hybridization may be a mechanism for generating novel and potentially beneficial holobiont phenotypes. Supporting such a conclusion, the correlations that we find between hybrid microbiota and the hybrid niche indicate that hybridization might change host microbiota in ways that promote a shift or an expansion in host niche space. If true, hybrid microbiota restructuring may underly ecological release from progenitors. This, in turn, could drive evolutionary diversification. Using our system as an example, we elaborate on the evolutionary implications of host hybridization within the context of holobiont theory and then outline the next steps for understanding the role of hybridization in holobiont research. Video Abstract.

In this paper, we explore the effects of hybridization on the gut (cloacal) and skin microbiota in an ecologically successful hybrid lizard, Aspidoscelis neomexicanus. Specifically, we test the hypothesis that hybrid lizards have host-associated (HA) microbiota traits strongly differentiated from their progenitor species. Across numerous hybrid microbiota phenotypes, we find widespread evidence of transgressive segregation. Further, microbiota restructuring broadly correlates with niche restructuring during hybridization. This suggests a relationship between HA microbiota traits and ecological success.