Incipient hybrid inferiority between recently introduced, diverging dung beetle populations

Abstract

Abstract Understanding why and how certain clades emerge as speciation hotspots is a fundamental objective of evolutionary biology. Here we investigate divergences between exotic Onthophagus taurus, a dung beetle introduced into the USA and Australia in the 1970s, as a potential model for the widespread recent speciation events characterizing the genus Onthophagus. To do so, we hybridized O. taurus derived from Eastern US (EUS) and Western Australian (WA) populations, and assessed fitness-relevant trait expression in first- and second-generation hybrids. We found that dams invest more in offspring provisioning when paired with a sire from the same population, and that WA dams crossed with EUS sires produce smaller and lighter F1 hybrids, with an unexpectedly male-biased sex ratio. Furthermore, fewer F2 hybrids with vertically inherited WA cytoplasm and microbiome emerged compared with WA backcrosses with WA cytoplasm/microbiome, suggesting that combinations of nuclear genome, cytoplasm and/or microbiome may contribute to hybrid viability. Lastly, we document a dominance of WA genotypes over body size at the point of inflection between minor and major male morphs, a trait of significance in mate competition, which has diverged remarkably between these populations. We discuss our results in light of the evolutionary ecology of onthophagine beetles and the role of developmental evolution in clade diversification.