ABSTRACT
Through niche construction, organisms modify their environments in ways that can alter how selection acts on themselves and their offspring. However, the role of niche construction in shaping developmental and evolutionary trajectories, and its importance for population divergences and local adaptation, remains largely unclear. In this study, we manipulated both maternal and larval niche construction and measured the effects on fitness-relevant traits in two rapidly diverging populations of the bull-headed dung beetle, Onthophagus taurus. We find that both types of niche construction enhance adult size, peak larval mass, and pupal mass, which when compromised lead to a synergistic decrease in survival. Furthermore, for one measure, duration of larval development, we find that the two populations have diverged in their reliance on niche construction: larval niche construction appears to buffer against compromised maternal niche construction only in beetles from Western Australia, but not in beetles from the Eastern United States. We discuss our results in the context of rapid adaptation to novel conditions and the role of niche construction therein.
Subject(s)
Biological Evolution , Coleoptera/physiology , Animals , Coleoptera/growth & development , Female , Larva/growth & development , Larva/physiology , Longevity , Male , Sex CharacteristicsABSTRACT
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 genus Onthophagus, 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.
Subject(s)
Adaptation, Biological , Biological Evolution , Coleoptera/physiology , Gene Regulatory Networks , Animals , Coleoptera/genetics , Coleoptera/growth & development , Life History TraitsABSTRACT
Niche construction occurs when organisms modify their environments and alter selective conditions 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 to which environmental modifications shape developmental and fitness outcomes, how their influences may differ among species and identify the underlying proximate mechanisms. Here, we experimentally eliminate environmental modifications from the developmental environment of Onthophagus dung beetles. We show that these modifications (1) differentially influence growth 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.
Subject(s)
Biological Evolution , Coleoptera/growth & development , Coleoptera/physiology , Animals , Coleoptera/genetics , Female , Larva/growth & development , Male , Phenotype , Reproduction , Sex CharacteristicsABSTRACT
To complete their development, diverse animal species rely on the presence of communities of symbiotic microbiota that are vertically transmitted from mother to offspring. In the dung beetle genus Onthophagus, newly hatched larvae acquire maternal gut symbionts by the consumption of a maternal fecal secretion known as the pedestal. Here, we investigate the role of pedestal symbionts in mediating the normal development of Onthophagus gazella. Through the stepwise removal of environmental and maternal sources of microbial inoculation, we find that pedestal microbiota can enhance both overall growth and developmental rate in O. gazella. Further, we find that the beneficial effects of symbionts on developmental outcomes are amplified in the presence of ecologically relevant temperature and desiccation stressors. Collectively, our results suggest that the pedestal may provide an adaptive function by transmitting beneficial microbiota to developing dung beetle larvae and that the importance of microbiota for developmental and fitness outcomes may be context dependent.
Subject(s)
Coleoptera/growth & development , Coleoptera/microbiology , Microbiota , Symbiosis , Animals , Feces/microbiology , Hawaii , Larva/growth & developmentABSTRACT
Resource allocation trade-offs arise when developing organs are in competition for a limited pool of resources to sustain growth and differentiation. Such competition may constrain the maximal size to which structures can grow and may force a situation in which the evolutionary elaboration of one structure may only be possible at the expense of another. However, recent studies have called into question both the consistency and evolutionary importance of resource allocation trade-offs. This study focuses on a well-described trade-off between the horns and eyes of Onthophagus beetles and assesses the degree to which it is influenced by genetic, developmental and ecological conditions. Contrary to expectations, we observed that trade-off signatures (i) were mostly absent within natural populations, (ii) mostly failed to match naturally evolved divergences in horn investment among populations, (iii) were subject to differential changes in F1 populations derived from divergent field populations and (iv) remained largely unaffected by developmental genetic manipulations of horn investment. Collectively, our results demonstrate that populations subject to different ecological conditions exhibit different patterns of, and differential plasticity in, resource allocation. Further, variation in ecological conditions, rather than canalized developmental mechanisms, may determine whether and to what degree morphological structures engage in resource allocation trade-offs.
Subject(s)
Coleoptera/physiology , Gene Expression Regulation , Insect Proteins/genetics , Phenotype , RNA Interference , Animals , Coleoptera/genetics , Coleoptera/growth & development , Female , Insect Proteins/metabolism , Larva/growth & development , Larva/physiology , MaleABSTRACT
Environment-responsive development contributes significantly to the phenotypic variation visible to selection and as such possesses the potential to shape evolutionary trajectories. However, evaluation of the contributions of developmental plasticity to evolutionary diversification necessitates an understanding of the developmental mechanisms underpinning plastic trait expression. We investigated the role of serotonin signaling in the regulation and evolution of horn polyphenism in the beetle genus Onthophagus. Specifically, we assessed the role of serotonin in development by determining whether manipulating serotonin biosynthesis during the larval stage alters body size, developmental rate, and the formation of relative adult trait size in traits characterized by minimal (genitalia), moderate (elytra), and pronounced (horns) nutrition-responsive development in O. taurus. Second, we assessed serotonin's role in evolution by replicating a subset of our approaches across four species reflecting ancestral as well as derived conditions. Lastly, we employed immunohistochemical approaches to begin assessing whether serotonin may be acting via the endocrine or nervous system. Our results show that pharmacological manipulation of serotonin signaling affects overall size, developmental rate, and the body size threshold separating alternate male morphs. Threshold body sizes were affected across species, regardless of the severity of horn polyphenism, and independent of the precise morphological location of horns. However, histological assessments suggest it is unlikely serotonin functions as a neurotransmitter and instead may rely on other mechanisms that remain to be identified. We discuss the most important implications of our results for our understanding of the evolution of and through plasticity in horned beetles and beyond.
Subject(s)
Adaptation, Physiological , Coleoptera/growth & development , Serotonin/metabolism , Animal Nutritional Physiological Phenomena , Animals , Body Size/drug effects , Coleoptera/drug effects , Larva/drug effects , Larva/growth & development , MaleABSTRACT
The oncometabolite L-2-hydroxyglutarate (L-2HG) is considered an abnormal product of central carbon metabolism that is capable of disrupting chromatin architecture, mitochondrial metabolism, and cellular differentiation. Under most circumstances, mammalian tissues readily dispose of this compound, as aberrant L-2HG accumulation induces neurometabolic disorders and promotes renal cell carcinomas. Intriguingly, Drosophila melanogaster larvae were recently found to accumulate high L-2HG levels under normal growth conditions, raising the possibility that L-2HG plays a unique role in insect metabolism. Here we explore this hypothesis by analyzing L-2HG levels in 18 insect species. While L-2HG was present at low-to-moderate levels in most of these species (<100 pmol/mg; comparable to mouse liver), dipteran larvae exhibited a tendency to accumulate high L-2HG concentrations (>100 pmol/mg), with the mosquito Aedes aegypti, the blow fly Phormia regina, and three representative Drosophila species harboring concentrations that exceed 1 nmol/mg - levels comparable to those measured in mutant mice that are unable to degrade L-2HG. Overall, our findings suggest that one of the largest groups of animals on earth commonly generate high concentrations of an oncometabolite during juvenile growth, hint at a role for L-2HG in the evolution of dipteran development, and raise the possibility that L-2HG metabolism could be targeted to restrict the growth of key disease vectors and agricultural pests.
Subject(s)
Aedes/metabolism , Calliphoridae/metabolism , Drosophila/metabolism , Glutarates/metabolism , Aedes/growth & development , Animals , Calliphoridae/growth & development , Drosophila/growth & development , Larva/growth & development , Larva/metabolismABSTRACT
Exposure to environmental variation is a characteristic feature of normal development, one that organisms can respond to during their lifetimes by actively adjusting or maintaining their phenotype in order to maximize fitness. Plasticity and robustness have historically been studied by evolutionary biologists through quantitative genetic and reaction norm approaches, while more recent efforts emerging from evolutionary developmental biology have begun to characterize the molecular and developmental genetic underpinnings of both plastic and robust trait formation. In this review, we explore how our growing mechanistic understanding of plasticity and robustness is beginning to force a revision of our perception of both phenomena, away from our conventional view of plasticity and robustness as opposites along a continuum and toward a framework that emphasizes their reciprocal, constructive, and integrative nature. We do so in three sections. Following an introduction, the first section looks inward and reviews the genetic, epigenetic, and developmental mechanisms that enable organisms to sense and respond to environmental conditions, maintaining and adjusting trait formation in the process. In the second section, we change perspective and look outward, exploring the ways in which organisms reciprocally shape their environments in ways that influence trait formation, and do so through the lens of behavioral plasticity, niche construction, and host-microbiota interactions. In the final section, we revisit established plasticity and robustness concepts in light of these findings, and highlight research opportunities to further advance our understanding of the causes, mechanisms, and consequences of these ubiquitous, and interrelated, phenomena.
ABSTRACT
Scaling relationships play critical roles in defining biological shape, trait functionality, and species characteristics, yet the developmental basis of scaling and its evolution remain poorly resolved in most taxa. In the horned beetle genus Onthophagus, scaling relationships of most traits are largely comparable across many species, however, the morphology and scaling of horns, a recent evolutionary invention, has diversified dramatically, ranging from modestly to highly positively linear to more complex sigmoidal allometries. Through a series of transcriptomic screens and gene function assays, the doublesex, hedgehog, insulin, and serotonin signaling pathways have recently been implicated in the regulation of amplitude, slope, and threshold location of the highly sigmoidal horn allometry in O. taurus. These and other findings suggest that co-option of these pathways into the regulation of horn development may have been critical in the evolutionary transitions from isometric to positively allometric to sigmoidal allometries in Onthophagus, thereby contributing to the extraordinary diversification of one of the most species-rich genera in the animal kingdom.
Subject(s)
Biological Evolution , Coleoptera/anatomy & histology , Coleoptera/physiology , Gene Expression Regulation, Developmental , Animals , Body Size/genetics , Coleoptera/genetics , Organ Size/genetics , Sex CharacteristicsABSTRACT
The elaboration of exaggerated, sexually selected weapons and ornaments often comes at a cost to other traits. For instance, by sustaining the growth of an exaggerated weapon during development, shared and limited resources such as morphogens, growth factors, and nutrients may become depleted and limit the size to which other structures can grow. Such interactions are characteristic of resource allocation trade-offs, which can constrain the production of phenotypic variation and bias evolutionary trajectories. Across many species of Onthophagus beetles, males produce extravagant horns that are used as weapons in male-male competition over mates. Previous studies have reported resource allocation trade-offs between horns and both proximally and distally developing structures. However, more recent studies have largely failed to recover these patterns, leading to the hypothesis that trade-offs may manifest only in certain species, populations, or environmental conditions. Here, we investigate (i) patterns of resource allocation into horns, eyes, and genitalia in Onthophagus gazella and O. taurus, and assess (ii) how these patterns of resource allocation are influenced by nutrient stress during larval development. We find that nutrient stress alters patterns of resource allocation within and among traits, but recover a trade-off only in the species that invests most heavily into horn production (O. taurus), and in individuals of that species that invested a disproportionately large or small amount of resources into horn growth. These results suggest that resource allocation trade-offs may not be as prevalent as previously described, and that their presence and magnitude may instead be highly context dependent.