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1. Microbial symbionts play a crucial role in the development, health, and homeostasis of their hosts. However, the eco‐evolutionary conditions shaping these relationships and the evolutionary scale at which host–microbiome interactions may diverge warrant further investigation, especially in non‐model systems. This study examines the impact of reciprocal gut microbiome transplants between two ecologically very similar, sympatric, and syntopic dung beetle sister species. 2.Onthophagus vaccaandOnthophagus mediuswere specifically used to compare the growth, development, and fitness outcomes of individuals that were either (i) reared in the presence of a microbiome provided by a mother of the same species (“self‐inoculated”), (ii) forced to develop with a microbiome derived from a heterospecific mother (“cross‐inoculated”), or (iii) reared without a maternally transmitted microbiome. 3. This study found that individuals reared in the absence of a maternally derived gut microbiome incur detrimental changes in survival, as well as in several metrics signalling normative development. Furthermore, such negative effects are only partly rescued through inoculation with a heterologous microbiome. 4. Collectively, this study's results suggest that inoculation with a species‐specific, maternally transmitted microbiome is critical for normative development, that the significance of maternally derived microbiota for host survival differs across species, and that the phenotypic outcomes resulting from host–microbiome interactions may diverge even between closely related, ecologically similar host species. 

Abstract Developmental processes transduce diverse influences during phenotype formation, thereby biasing and structuring amount and type of phenotypic variation available for evolutionary processes to act on. The causes, extent, and consequences of this bias are subject to significant debate. Here we explore the role of developmental bias in contributing to organisms’ ability to innovate, to adapt to novel or stressful conditions, and to generate well integrated, resilient phenotypes in the face of perturbations. We focus our inquiry on one taxon, the horned dung beetle genusOnthophagus, and review the role developmental bias might play across several levels of biological organization: (a) gene regulatory networks that pattern specific body regions; (b) plastic developmental mechanisms that coordinate body wide responses to changing environments and; (c) developmental symbioses and niche construction that enable organisms to build teams and to actively modify their own selective environments. We posit that across all these levels developmental bias shapes the way living systems innovate, adapt, and withstand stress, in ways that can alternately limit, bias, or facilitate developmental evolution. We conclude that the structuring contribution of developmental bias in evolution deserves further study to better understand why and how developmental evolution unfolds the way it does.