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Evidence of Developmental Niche Construction in Dung Beetles: Effects on Growth, Scaling and Reproductive Success

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Evidence of Developmental Niche Construction in Dung Beetles: Effects on Growth, Scaling and Reproductive Success Ecology Letters, (2017) doi: 10.1111/ele.12830 LETTER Evidence of developmental niche construction in dung beetles: effects on growth, scaling and reproductive success Abstract Daniel B. Schwab,* Sofia Casasa Niche construction occurs when organisms modify their environments and alter selective condi- and Armin P. Moczek tions through their physiology and behaviours. Such modifications can bias phenotypic variation and enhance organism–environment fit. Yet few studies exist that experimentally assess the degree Department of Biology, Indiana to which environmental modifications shape developmental and fitness outcomes, how their influ- University, Bloomington, IN 47405, ences may differ among species and identify the underlying proximate mechanisms. Here, we USA experimentally eliminate environmental modifications from the developmental environment of *Correspondence: E-mail: Onthophagus dung beetles. We show that these modifications (1) differentially influence growth [email protected] among species, (2) consistently shape scaling relationships in fitness-related traits, (3) are necessary for the maintenance of sexual dimorphism, (4) influence reproductive success among females of at least one species and (5) implicate larval cultivation of an external rumen as a possible mechanism for environmental modification. Our results present evidence that Onthophagus larvae engage in niche construction, and that this is a fundamental component of beetle development and fitness. Keywords developmental plasticity, developmental symbiosis, ecological inheritance, horned beetles, Onthophagus. Ecology Letters (2017) empirically and theoretically in, diverse research programs, INTRODUCTION such as density-dependent selection, sexual selection and social- Understanding how organisms come to complement their and co-evolutionary theory, all of which are predicated on an environments to maintain or enhance their fitness has been a understanding of how interactions between individuals, poten- long-standing focus of evolutionary biology. For many organ- tial mates, social groups and other species influence the out- isms, this complementarity is achieved by modifying their comes of selection (Scott-Phillips et al. 2014). In addition, the traits either developmentally through phenotypic plasticity or field of eco-evolutionary feedbacks has begun to demonstrate alternatively through adaptive evolution (Zimmer & Emlen how organismal (e.g. predator–prey) interactions produce feed- 2013). At the same time, rather than adjusting their traits to back loops between ecological and evolutionary dynamics, gen- fit their selective environment, many organisms can physiolog- erating a conceptual framework that is independent of, though ically or behaviourally modify their selective environment to broadly overlapping with, NCT (Kylafis & Loreau 2008; Post better suit their traits through the process of niche construction & Palkovacs 2009; Odling-Smee et al. 2013; Matthews et al. (Odling-Smee et al. 2003; Laland et al. 2015). Niche construc- 2014). Where NCT diverges from other frameworks, however, tion is operationally defined as occurring when two criteria is in its explicit emphasis on environment-modifying abilities as are fulfilled: (1) an organism significantly modifies environ- sources of individual phenotypic variation, as an alternate mental conditions, and (2) these organism-mediated environ- route to adaptation and as an avenue for non-genetic inheri- mental modifications influence selection pressures on a tance in those cases in which modified environments are passed recipient of niche construction (Matthews et al. 2014). This on to subsequent generations. Here, we use NCT as a frame- has the potential to lead to evolution through niche construc- work for explicitly exploring the phenomenon of developmental tion when a third criterion is met, namely (3) that there is a niche construction, and evaluate whether environment-modify- detectable genetic change in the recipient population that ing behaviours of dung beetle larvae fulfil the two criteria alters the relationship between phenotype distribution and fit- needed to qualify as niche constructors. ness variation (Matthews et al. 2014). Developmental niche construction manifests in diverse forms Niche construction theory (NCT) is not the first conceptual across an array of taxa, but is most often expressed when framework to emphasise the environment-modifying abilities organisms alter ontogenetic environments via chemical excre- of organisms, nor the potential feedbacks to selective pressures tions or through the construction of physical structures such as that arise from such interactions: for instance, the environ- dams, burrows or pupal cases. One common function of these ment-constructing abilities of corals and earthworms were modifications is to buffer developing organisms against other- highlighted at least as early as Darwin (1842, 1881), and wise challenging environmental conditions. For instance, gall- diverse other cases have since been described for many taxa flies induce gall formation on plants, providing the fly with (documented in Odling-Smee et al. 2003). Further, alteration nutrition as well as protection from parasitoids and avian of selective conditions due to environment-modifying activities predators (Abrahamson et al. 1989). In addition, organisms are central to, and have been explored in depth both may depend on the physiological properties of symbionts to © 2017 John Wiley & Sons Ltd/CNRS 2 D. B. Schwab et al. Letter generate suitable developmental and nutritional environments, Here, we use a novel method for suppressing all known lar- as in larval woodwasps that obtain their sole source of dietary val modifications to the brood ball environment to evaluate sterols from maternally provisioned fungi (Thompson et al. (1) whether larvae indeed engage in niche construction and (2) 2013). In each of these cases, environmental modifications the extent to which environmental modifications are central to become fundamental to ensuring the normal development of normal development across three Onthophagus species. We the organisms that exert them (Laland et al. 2008). first test the prediction that these modifications enhance larval While developmental niche construction is therefore a com- growth, larval survival and adult reproductive success. Next, mon characteristic of organismal development and has the we investigate whether larval modifications alter morphologi- potential to affect evolutionary outcomes, substantial empiri- cal scaling relationships, including the nature and degree of cal work remains necessary, for the following reasons. First, sexual dimorphism, in three environmentally responsive traits. while extensive work exists documenting the ecological and Then, to evaluate if and to what extent the effect of environ- evolutionary significance of soil-modifying properties of plants mental modifications on growth outcomes has diverged and their microbial partners (reviewed in Putten et al. 2013; among closely related species, we compare their effect sizes Pii et al. 2015), few animal model systems have been devel- among three Onthophagus species. Finally, to better charac- oped where the mechanisms of developmental niche construc- terise the known mechanisms by which larvae modify their tion, and the environmental variables being modified, are well brood ball environment, we generate a community-level physi- understood and experimentally manipulable. Understanding ological profile of the faecal microbiota that larvae spread these mechanisms may elucidate not only how organisms throughout the brood ball, testing the prediction that this modify their ontogenetic environment, but also how these community is enriched for potentially beneficial microbes cap- mechanisms may be selected upon to influence evolutionary able of metabolising recalcitrant, dung-associated carbon sub- trajectories (Odling-Smee et al. 2003). Second, despite the fact strates (e.g. cellobiose). In combination, our study that the outcomes of development are often highly environ- demonstrates that larval brood ball modifications are (1) a mentally contingent, whether and how niche constructed envi- normal, fitness-determining component of dung beetle devel- ronments reciprocally shape norms of reaction across opment necessary for (2) the maintenance and expression of organismal traits are poorly understood. Finally, while it is sexual dimorphism, and whose (3) effects on growth and generally assumed that niche constructing traits and their development are variable among species, thereby providing associated impacts on development and fitness exhibit genetic evidence that Onthophagus larvae engage in niche construc- variation, much of the empirical literature has focused on tion. traits that are largely functionally invariant among popula- tions or species, such as the construction of termite mounds or bird nests (Saltz & Nuzhdin 2014). Thus, little is known MATERIALS AND METHODS about if and how individuals, populations and species vary in Beetle husbandry and manipulation of brood ball modifications niche constructing traits, and how this variation shapes phenotypic variation and fitness in natural environments. Brood balls from O. taurus, O. gazella and O. sagittarius were Larval dung beetles in the genus Onthophagus present a generated as described previously (Shafiei et al. 2001; but also promising model system for addressing the study of niche con- see supplementary materials and methods in the Supporting struction. Onthophagus larvae spend
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