Don’t stand so close to me: Microbiota‐facilitated enemy release dynamics in introduced Onthophagus taurus dung beetles

Abstract

Microbial symbionts can influence their hosts in stunningly diverse ways. Emerging research suggests that an underappreciated facet of these relationships is the influence microbes can have on their host's responses to novel, or stressful, environmental conditions. We sought to address these and related questions in populations resulting from the recent introduction and subsequent rapid range expansion of Onthophagus taurus dung beetles. Specifically, we manipulated both microbial communities and rearing temperature to detect signatures of developmental and life history differentiation in response to the local thermal conditions in two populations derived from the southern most (Florida) and northern most (Michigan) extremes of the exotic Eastern U.S. range of O. taurus. We then sought to determine the contributions, if any, of host-associated microbiota to this differentiation. We found that when reared under common garden conditions individuals from Florida and Michigan populations differed significantly in developmental performance measures and life history traits, consistent with population divergence. At the same time, and contrary to our predictions, we failed to find support for the hypothesis that animals perform better if reared at temperatures that match their location of origin and that performance differences may be mediated by host-associated microbiota. Instead, we found that microbiome swapping across host populations improved developmental performance in both populations, consistent with enemy release dynamics. We discuss the implications of our results for our understanding of the rapid spread of exotic O. taurus through the Eastern United States and the significance of symbiosis in host responses to novel environmental conditions more broadly.

Vertically inherited microbiota and environment modifying behaviours conceal genetic variation in dung beetle life history

“…Previous work indicated differences among species or populations in the effects of brood ball modification and the vertical transmission of microbiomes on dung beetle performance [7,30,32]. Here, we find that the genetic values in the control environment do not perfectly predict the genetic values in a manipulated environment.…”

“…In so doing, the mother's gut microbiome is transmitted vertically to its offspring [27]. These vertically transmitted microbial communities have been shown to be host species-and population-specific [28] and to yield deleterious fitness consequences if withheld [7,[29][30][31]. The dung beetle microbiome contains a diverse set of microbial taxa primarily belonging to Enterobacteriaceae, Pseudomonadaceae and Comamonadaceae [27].…”

Host genomic variation shapes gut microbiome diversity in threespine stickleback fish

“…Importantly, external fertilization and early surface sterilization of embryos via gnotobiotic techniques developed for stickleback 25 allowed us to control for vertical transfer of microbes and to create a common conventional starting point for microbial colonization among individuals. Germ-free derivation has also been leveraged to understand host genetic contributions to microbiome attributes in Drosophila 67 , dung beetles 68 , mice 69 , and zebrafish 64 , although some of these studies relied on inbred lines or induced mutations, which places limitations on their ability to recapitulate and interrogate the landscapes of genetic variation often observed in natural populations. The design of our current study included both crucial elements: genetic variation sampled recently from natural stickleback populations coupled with a highly controlled, standardized environment.…”

Promises and limits of an agency perspective in evolutionary developmental biology

“…More generally, the potential value for evo devo research on host–microbiome interactions from an agency perspective is similar to the arguments made for niche construction above: host–microbiome interactions have the potential to causally influence development, create alternate routes of inheritance in those cases in which microbial partners are vertically transmitted, contribute to (context‐dependent) heritable variation in populations, and provide opportunities for differentiation and diversification among populations and species. Already, a growing number of case studies support such contributions in diverse taxa (insects: Feldhaar, 2011; Lemoine et al, 2020; dung beetles: Parker & Moczek, 2020; Parker et al, 2019, 2020, 2021; Schwab et al, 2016; flies: Morimoto et al, 2017; Nguyen et al, 2020; stickleback fish: Smith et al, 2015; see also Corbin et al, 2017; Renoz et al, 2019).…”