125 research outputs found

    Pupal remodeling and the evolution and development of alternative male morphologies in horned beetles

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    <p>Abstract</p> <p>Background</p> <p>How novel morphological traits originate and diversify represents a major frontier in evolutionary biology. Horned beetles are emerging as an increasingly popular model system to explore the genetic, developmental, and ecological mechanisms, as well as the interplay between them, in the genesis of novelty and diversity. The horns of beetles originate during a rapid growth phase during the prepupal stage of larval development. Differential growth during this period is either implicitly or explicitly assumed to be the sole mechanism underlying differences in horn expression within and between species. Here I focus on male horn dimorphisms, a phenomenon at the center of many studies in behavioral ecology and evolutionary development, and quantify the relative contributions of a previously ignored developmental process, pupal remodeling, to the expression of male dimorphism in three horned beetle species.</p> <p>Results</p> <p>Prepupal growth is not the only determinant of differences in male horn expression. Instead, following their initial prepupal growth phase, beetles may be extensively remodeled during the subsequent pupal stage in a sex and size-dependent manner. Specifically, male dimorphism in the three <it>Onthophagus </it>species studied here was shaped not at all, partly or entirely by such pupal remodeling rather than differential growth, suggesting that pupal remodeling is phylogenetically widespread, evolutionarily labile, and developmentally flexible.</p> <p>Conclusion</p> <p>This study is the first to document that male dimorphism in horned beetles is the product of two developmentaly dissociated processes: prepupal growth and pupal remodeling. More generally, adult morphology alone appears to provide few clues, if any, as to the relative contributions of both processes to the expression of alternative male morphs, underscoring the importance of developmental studies in efforts aimed at understanding the evolution of adult diversity patterns.</p

    Development of functional ectopic compound eyes in scarabaeid beetles by knockdown of orthodenticle

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    Complex traits like limbs, brains, or eyes form through coordinated integration of diverse cell fates across developmental space and time, yet understanding how complexity and integration emerge from uniform, undifferentiated precursor tissues remains limited. Here, we use ectopic eye formation as a paradigm to investigate the emergence and integration of novel complex structures following massive ontogenetic perturbation. We show that down-regulation via RNAi of a single head patterning gene—orthodenticle—induces ectopic structures externally resembling compound eyes at the middorsal adult head of both basal and derived scarabaeid beetle species (Onthophagini and Oniticellini). Scanning electron microscopy documents ommatidial organization of these induced structures, while immunohistochemistry reveals the presence of rudimentary ommatidial lenses, crystalline cones, and associated neural-like tissue within them. Further, RNA-sequencing experiments show that after orthodenticle down-regulation, the transcriptional signature of the middorsal head—the location of ectopic eye induction—converges onto that of regular compound eyes, including up-regulation of several retina-specific genes. Finally, a light-aversion behavioral assay to assess functionality reveals that ectopic compound eyes can rescue the ability to respond to visual stimuli when wild-type eyes are surgically removed. Combined, our results show that knockdown of a single gene is sufficient for the middorsal head to acquire the competence to ectopically generate a functional compound eye-like structure. These findings highlight the buffering capacity of developmental systems, allowing massive genetic perturbations to be channeled toward orderly and functional developmental outcomes, and render ectopic eye formation a widely accessible paradigm to study the evolution of complex systems.Fil: Zattara, Eduardo Enrique. Indiana University; Estados Unidos. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Patagonia Norte. Instituto de Investigaciones en Biodiversidad y Medioambiente. Universidad Nacional del Comahue. Centro Regional Universidad Bariloche. Instituto de Investigaciones en Biodiversidad y Medioambiente; ArgentinaFil: Macagno, Anna L. M.. Indiana University; Estados UnidosFil: Busey, Hannah A.. Indiana University; Estados UnidosFil: Moczek, Armin P.. Indiana University; Estados Unido

    Threshold Evolution in Exotic Populations of a Polyphenic Beetle

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    Polyphenic development is thought to play an important role in the evolution of phenotypic diversity and morphological novelties, yet the evolution of polyphenisms has rarely been documented in natural populations. Here we compare the morphologies of male dung beetles (Onthophagus taurus; Coleoptera: Scarabaeidae) from populations introduced to Australia and the eastern United States. Males in this species express two alternative morphologies in response to larval feeding conditions. Males encountering favourable conditions grow larger than a threshold body size and develop a pair of horns on their heads, whereas males that encounter poor conditions do not reach this threshold size and remain hornless. Australian and US populations did not differ in overall body size ranges, but exhibited significant differences in the location of the critical body size threshold that separates alternative male morphs. Australian males remained hornless at much larger body sizes than males in US populations, resulting in substantial and significant differences in the average body size-horn length allometry between exotic populations, as well as significant differences in morph ratios. The phenotypic divergence observed between field populations was maintained in laboratory populations after two generations under identical environmental conditions, suggesting a genetic basis to allometric divergence in these populations. Divergence between exotic O. taurus populations was of a magnitude and kind typically observed between species. We use our results to examine potential causes of allometric divergence in onthophagine beetles, and discuss the evolutionary potential of threshold traits and polyphenic development in the origin of morphological and behavioural diversity

    EST and microarray analysis of horn development in Onthophagus beetles

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    <p>Abstract</p> <p>Background</p> <p>The origin of novel traits and their subsequent diversification represent central themes in evo-devo and evolutionary ecology. Here we explore the genetic and genomic basis of a class of traits that is both novel and highly diverse, in a group of organisms that is ecologically complex and experimentally tractable: horned beetles.</p> <p>Results</p> <p>We developed two high quality, normalized cDNA libraries for larval and pupal <it>Onthophagus taurus </it>and sequenced 3,488 ESTs that assembled into 451 contigs and 2,330 singletons. We present the annotation and a comparative analysis of the conservation of the sequences. Microarrays developed from the combined libraries were then used to contrast the transcriptome of developing primordia of head horns, prothoracic horns, and legs. Our experiments identify a first comprehensive list of candidate genes for the evolution and diversification of beetle horns. We find that developing horns and legs show many similarities as well as important differences in their transcription profiles, suggesting that the origin of horns was mediated partly, but not entirely, by the recruitment of genes involved in the formation of more traditional appendages such as legs. Furthermore, we find that horns developing from the head and prothorax differ in their transcription profiles to a degree that suggests that head and prothoracic horns are not serial homologs, but instead may have evolved independently from each other.</p> <p>Conclusion</p> <p>We have laid the foundation for a systematic analysis of the genetic basis of horned beetle development and diversification with the potential to contribute significantly to several major frontiers in evolutionary developmental biology.</p

    On the Reciprocally Causal and Constructive Nature of Developmental Plasticity and Robustness

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    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

    Adaptive maternal behavioral plasticity and developmental programming mitigate the transgenerational effects of temperature in dung beetles

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    Phenotypic plasticity allows organisms to cope with rapid environmental change. Yet exactly when during ontogeny plastic responses are elicited, whether plastic responses produced in one generation influence phenotypic variation and fitness in subsequent generations, and the role of plasticity in shaping population divergences, remains overall poorly understood. Here, we use the dung beetle Onthophagus taurus to assess plastic responses to temperature at several life stages bridging three generations and compare these responses across three recently diverged populations. We find that beetles reared at hotter temperatures grow less than those reared at mild temperatures, and that this attenuated growth has transgenerational consequences by reducing offspring size and survival in subsequent generations. However, we also find evidence that plasticity may mitigate these consequences in two ways: 1) mothers modify the temperature of their offspring's developmental environment via behavioral plasticity and 2) in one population, offspring exhibit accelerated growth when exposed to hot temperatures during very early development (‘developmental programming’). Lastly, our study reveals that offspring responses to temperature diverged among populations in fewer than 100 generations, possibly in response to range-specific changes in climatic or social conditions.Fil: Macagno, Anna L. M.. Indiana University; Estados UnidosFil: Zattara, Eduardo Enrique. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Patagonia Norte. Instituto de Investigaciones en Biodiversidad y Medioambiente. Universidad Nacional del Comahue. Centro Regional Universidad Bariloche. Instituto de Investigaciones en Biodiversidad y Medioambiente; Argentina. Indiana University; Estados UnidosFil: Ezeakudo, Onye. Homestead High School; Estados UnidosFil: Moczek, Armin P.. Indiana University; Estados UnidosFil: Ledón Rettig, Cristina. Indiana University; Estados Unido

    Gene discovery in the horned beetle Onthophagus taurus

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    <p>Abstract</p> <p>Background</p> <p>Horned beetles, in particular in the genus <it>Onthophagus</it>, are important models for studies on sexual selection, biological radiations, the origin of novel traits, developmental plasticity, biocontrol, conservation, and forensic biology. Despite their growing prominence as models for studying both basic and applied questions in biology, little genomic or transcriptomic data are available for this genus. We used massively parallel pyrosequencing (Roche 454-FLX platform) to produce a comprehensive EST dataset for the horned beetle <it>Onthophagus taurus</it>. To maximize sequence diversity, we pooled RNA extracted from a normalized library encompassing diverse developmental stages and both sexes.</p> <p>Results</p> <p>We used 454 pyrosequencing to sequence ESTs from all post-embryonic stages of <it>O. taurus. </it>Approximately 1.36 million reads assembled into 50,080 non-redundant sequences encompassing a total of 26.5 Mbp. The non-redundant sequences match over half of the genes in <it>Tribolium castaneum</it>, the most closely related species with a sequenced genome. Analyses of Gene Ontology annotations and biochemical pathways indicate that the <it>O. taurus </it>sequences reflect a wide and representative sampling of biological functions and biochemical processes. An analysis of sequence polymorphisms revealed that SNP frequency was negatively related to overall expression level and the number of tissue types in which a given gene is expressed. The most variable genes were enriched for a limited number of GO annotations whereas the least variable genes were enriched for a wide range of GO terms directly related to fitness.</p> <p>Conclusions</p> <p>This study provides the first large-scale EST database for horned beetles, a much-needed resource for advancing the study of these organisms. Furthermore, we identified instances of gene duplications and alternative splicing, useful for future study of gene regulation, and a large number of SNP markers that could be used in population-genetic studies of <it>O. taurus </it>and possibly other horned beetles.</p

    Shape - but Not Size - Codivergence between Male and Female Copulatory Structures in Onthophagus Beetles

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    Genitalia are among the fastest evolving morphological traits in arthropods. Among the many hypotheses aimed at explaining this observation, some explicitly or implicitly predict concomitant male and female changes of genital traits that interact during copulation (i.e., lock and key, sexual conflict, cryptic female choice and pleiotropy). Testing these hypotheses requires insights into whether male and female copulatory structures that physically interact during mating also affect each other's evolution and patterns of diversification. Here we compare and contrast size and shape evolution of male and female structures that are known to interact tightly during copulation using two model systems: (a) the sister species O. taurus (1 native, 3 recently established populations) and O. illyricus, and (b) the species-complex O. fracticornis-similis-opacicollis. Partial Least Squares analyses indicated very little to no correlation between size and shape of copulatory structures, both in males and females. Accordingly, comparing shape and size diversification patterns of genitalia within each sex showed that the two components diversify readily - though largely independently of each other - within and between species. Similarly, comparing patterns of divergence across sexes showed that relative sizes of male and female copulatory organs diversify largely independent of each other. However, performing this analysis for genital shape revealed a signature of parallel divergence. Our results therefore suggest that male and female copulatory structures that are linked mechanically during copulation may diverge in concert with respect to their shapes. Furthermore, our results suggest that genital divergence in general, and co-divergence of male and female genital shape in particular, can evolve over an extraordinarily short time frame. Results are discussed in the framework of the hypotheses that assume or predict concomitant evolutionary changes in male and female copulatory organs

    Genome of the Asian Longhorned Beetle (\u3cem\u3eAnoplophora glabripennis\u3c/em\u3e), a Globally Significant Invasive Species, Reveals Key Functional and Evolutionary Innovations at the Beetle-Plant Interface

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    Background: Relatively little is known about the genomic basis and evolution of wood-feeding in beetles. We undertook genome sequencing and annotation, gene expression assays, studies of plant cell wall degrading enzymes, and other functional and comparative studies of the Asian longhorned beetle, Anoplophora glabripennis, a globally significant invasive species capable of inflicting severe feeding damage on many important tree species. Complementary studies of genes encoding enzymes involved in digestion of woody plant tissues or detoxification of plant allelochemicals were undertaken with the genomes of 14 additional insects, including the newly sequenced emerald ash borer and bull-headed dung beetle. Results: The Asian longhorned beetle genome encodes a uniquely diverse arsenal of enzymes that can degrade the main polysaccharide networks in plant cell walls, detoxify plant allelochemicals, and otherwise facilitate feeding on woody plants. It has the metabolic plasticity needed to feed on diverse plant species, contributing to its highly invasive nature. Large expansions of chemosensory genes involved in the reception of pheromones and plant kairomones are consistent with the complexity of chemical cues it uses to find host plants and mates. Conclusions: Amplification and functional divergence of genes associated with specialized feeding on plants, including genes originally obtained via horizontal gene transfer from fungi and bacteria, contributed to the addition, expansion, and enhancement of the metabolic repertoire of the Asian longhorned beetle, certain other phytophagous beetles, and to a lesser degree, other phytophagous insects. Our results thus begin to establish a genomic basis for the evolutionary success of beetles on plants
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