Evolution and plasticity of morph‐specific integration in the bull‐headed dung beetle Onthophagus taurus

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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.

Section: Discussionmentioning

confidence: 99%

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

Parker

Moczek

2020

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“…To quantify adult tibia shape, we followed previously established protocols (Rohner et al, 2020). In brief, we removed both fore tibiae and photographed them using a digital camera (Scion, Frederick, MD, USA) mounted on a Leica MZ‐16 stereomicroscope (Bannockburn, IL, USA).…”

Section: Methodsmentioning

confidence: 99%

Evolutionary and plastic variation in larval growth and digestion reveal the complex underpinnings of size and age at maturation in dung beetles

Rohner

Moczek

2021

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Age and size at maturity are key life‐history components, yet the proximate underpinnings that mediate intra‐ and interspecific variation in life history remain poorly understood. We studied the proximate underpinnings of species differences and nutritionally plastic variation in adult size and development time in four species of dung beetles. Specifically, we investigated how variation in insect growth mediates adult size variation, tested whether fast juvenile growth trades‐off with developmental stability in adult morphology and quantified plastic responses of digestive systems to variation in food quality. Contrary to the common size–development time trade‐off, the largest species exhibited by far the shortest development time. Correspondingly, species diverged strongly in the shape of growth trajectories. Nutritionally plastic adjustments to growth were qualitatively similar between species but differed in magnitude. Although we expected rapid growth to induce developmental costs, neither instantaneous growth rates nor the duration of larval growth were related to developmental stability in the adult. This renders the putative costs of rapid growth enigmatic. We further found that larvae that encounter a challenging diet develop a larger midgut and digest more slowly than animals reared on a more nutritious diet. These data are consistent with the hypothesis that larvae invest into a more effective digestive system when exposed to low‐quality nutrition, but suggest that species may diverge readily in their reliance on these mechanisms. More generally, our data highlight the complex, and often hidden, relationships between immature growth and age and size at maturation even in ecologically similar species.

“…This tooth is the largest of all four tibial teeth and is much longer and broader in females compared to males (see Figure 1 ). Male head horns were photographed using a Pixelink PL‐D797CU‐T camera mounted on a Leica MZ 16 stereomicroscope and measured as the length of the outline between the eye and the tip of the horn (Rohner et al., 2020 ; also see Figure S1 ). Occasionally, prepupae position themselves in such a way that the development of one of the horns is impeded during pupal development, leading to characteristic deformations and asymmetries in horn morphology.…”

Section: Methodsmentioning

confidence: 99%

Vertically inherited microbiota and environment‐modifying behaviors indirectly shape the exaggeration of secondary sexual traits in the gazelle dung beetle

Rohner,

Moczek

2023

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Many organisms actively manipulate the environment in ways that feed back on their own development, a process referred to as developmental niche construction. Yet, the role that constructed biotic and abiotic environments play in shaping phenotypic variation and its evolution is insufficiently understood. Here, we assess whether environmental modifications made by developing dung beetles impact the environment‐sensitive expression of secondary sexual traits. Gazelle dung beetles both physically modify their ontogenetic environment and structure their biotic interactions through the vertical inheritance of microbial symbionts. By experimentally eliminating (i) physical environmental modifications and (ii) the vertical inheritance of microbes, we assess the degree to which (sym)biotic and physical environmental modifications shape the exaggeration of several traits varying in their degree and direction of sexual dimorphism. We expected the experimental reduction of a larva's ability to shape its environment to affect trait size and scaling, especially for traits that are sexually dimorphic and environmentally plastic. We find that compromised developmental niche construction indeed shapes sexual dimorphism in overall body size and the absolute sizes of male‐limited exaggerated head horns, the strongly sexually dimorphic fore tibia length and width, as well as the weakly dimorphic elytron length and width. This suggests that environmental modifications affect sex‐specific phenotypic variation in functional traits. However, most of these effects can be attributed to nutrition‐dependent plasticity in size and non‐isometric trait scaling rather than body‐size‐independent effects on the developmental regulation of trait size. Our findings suggest that the reciprocal relationship between developing organisms, their symbionts, and their environment can have considerable impacts on sexual dimorphism and functional morphology.