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WIREs Dev Biol
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Beetle horns and horned beetles: emerging models in developmental evolution and ecology

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Abstract Many important questions in developmental biology increasingly interface with related questions in other biological disciplines such as evolutionary biology and ecology. In this article, we review and summarize recent progress in the development of horned beetles and beetle horns as study systems amenable to the integration of a wide range of approaches, from gene function analysis in the laboratory to population ecological and behavioral studies in the field. Specifically, we focus on three key questions at the current interface of developmental biology, evolutionary biology and ecology: (1) the developmental mechanisms underlying the origin and diversification of novel, complex traits, (2) the relationship between phenotypic diversification and the diversification of genes and transcriptomes, and (3) the role of behavior as a leader or follower in developmental evolution. For each question we discuss how work on horned beetles is contributing to our current understanding of key issues, as well as highlight challenges and opportunities for future studies. WIREs Dev Biol 2013, 2:405–418. doi: 10.1002/wdev.81 For further resources related to this article, please visit the WIREs website.

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Examples of the exuberance and diversity of horn phenotypes across genera. From top to bottom: Phanaeus imperator, Onthophagus watanabei, Eupatorus gracilicornis, Trypoxylus (Allomyrina) dichotoma, Golofa claviger. (Reprinted after Ref 3. Copyright 2008 Armin Moczek)

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Divergences in the social context of male horn dimorphism appear to drive morphological divergences in exotic populations of Onthophagus taurus. (a and b) Alternative reproductive tactics of horned (solid arrow) and hornless (dashed arrow) males. Horned males guard (a) and fight over (b) access to tunnel entrances containing breeding females. Hornless males utilize non‐aggressive sneaking behaviors such as digging of interception tunnels (a, left dashed arrow), using naturally existing tunnel connections (a, right dashed arrow), or waiting as satellite males until guarding males are distracted in order to gain access to females (b, dashed arrow). Figures (a) and (b); reprinted with permission from Ref 39. Copyright 2009 Science Publishers. (c) Scaling relationship between body size (x‐axis) and horn length (y‐axis) in three exotic, geographically isolated populations. (d) Correlation between body size thresholds (x‐axis) and densities (y‐axis) in local populations across the same three exotic ranges. Theoretical models (see text) predict that body size thresholds (c) can diverge as a result of differences in local densities of competing males (d), i.e., high density populations exhibit higher size thresholds than low density populations. Data in (c) and (d); reprinted with permission from Ref 40. Copyright 2003 Oxford University Press.

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Example of a microarray study in horned beetles designed to identify similarities and differences in gene expression profiles between developing head horns, thoracic horns, and legs of the horned beetle O. taurus. (Reprinted after Ref 22. Copyright 2010 Armin Moczek). (a) Microarray experimental design. The pupal tissues used in this study are indicated in the upper panel, whereas the general array hybridization scheme is illustrated in the lower panel. Head horn (head), thoracic horn (thorax), and legs are labeled yellow, pink, and blue, respectively. RNA from each tissue was competitively hybridized with RNA from abdominal epithelium (abdomen, white). (b) Hierarchical clustering of differentially expressed genes indicates an overall high level of similarity in gene expression patterns between developing head and thoracic horns and, to a slightly lesser degree, legs. 1367 spots showed significant and differential expression, and are shown clustered based on their M‐values when compared to abdominal epithelium. Each row represents a single spot and each column represents the sample. Relative magnitude of gene expression level is indicated by color brightness; red indicates enriched compared to abdominal epithelium whereas green indicates depleted relative to abdominal epithelium. Bootstrap value was obtained after 5000 trials. Branch lengths represent relative distances between the samples. (c) Categorization of genes that exhibited significantly differential expression, illustrating the unique components of head‐ and thoracic horn transcriptomes. Significant differential expression was defined by a P‐value < 0.05 and > twofold difference in expression levels. Labels on each category represent tissue types (head = head horns, thorax = prothoracic horns, and legs = legs). Numbers indicated in the Venn diagram represent counts of non‐redundant sequences in each category. Numbers in parentheses indicate counts of sequences that showed enriched or depleted expression relative to abdominal epithelium, where: red = enriched, blue = depleted, and pink = mixed (i.e., enriched in thoracic horns and depleted in legs).

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Examples of RNAi‐mediated gene function analyses in horned beetles. (a)–(f) Proximo‐distal (P/D) axis patterning genes, (g)–(k) TGFβ‐signaling; (l)–(n) Hox genes. (a)–(f) Analysis of P/D axis patterning genes in O. taurus for dachshund (dac) (a, b), homothorax (hth) (c, d), and Distal‐less (Dll) (e, f). (a, c, e) RNAi results in characteristic phenotypes in traditional appendages also observed in other insect models (a = deletion of medial antenna; c = induction of ectopic T1 wings; e = loss of distal leg regions). (b, d, f) Effects on scaling relationship between body size (x‐axis) and horn length (y‐axis; Reprinted with permission from Ref 10. Copyright 2009 Proceedings of the National Academy of Sciences). (g)–(k) Down‐regulation of the TGFβ‐signaling pathway member Decapentaplegic (dpp) reduces horn growth in O. binodis. (g, h) Typical Onthophagus Dpp knock‐down phenotypes similar to those seen in other insects (g, notal cleft; h, leg deformation). (i, k) typical horn phenotype and allometry in control‐injected and RNAi individuals (Reprinted with permission from Ref 12. Copyright 2011 Springer Publishers). (l)–(n) Examples of Hox‐RNAi phenotypes in O. binodis. (l) labial‐to‐maxillary palp transformation (TF) following‐down regulation of Sex combs reduced (Scr). (m) Maxilla‐to‐leg transformation following maxillopedia‐RNAi. Phenotypes match those reported for other insects. (n) Scr‐RNAi does not affect (i) prepupal growth but alters (ii) pupal remodeling of thoracic horns in O. nigriventris (Reprinted with permission from Ref 11. Copyright 2011 Wiley Publishers and Moczek and Simonnet, unpublished).

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Schematic of thoracic horn development and summary of expression data for proximo‐distal patterning genes during horn formation from embryo to pupa. Colors indicate tissue types and regional relationships between immature and mature appendage. (Reprinted with permission from Ref 2. Copyright 2009 Elsevier/Academic Press)

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(a) Examples of alternative male morphs in Onthophagus taurus (top) and O. nigriventris (bottom). Large males are shown on the left and small males on the right. Note that females (not shown) are entirely hornless in both species. (b) Rare reversed sexual dimorphism in O. sagittarius. Males (shown on left) also lost ancestral male dimorphism. (Reprinted with permission from Ref 17. Copyright 2012 Hindawi Publishers)

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