Biomedical subjects

Armin P Moczek

Publications and source records attributed to Armin P Moczek.

7 recordsLinked to original sources

PubMed2006

Pupal remodeling and the development and evolution of sexual dimorphism in horned beetles.

Horns or hornlike structures in beetles have become an increasingly popular study system for exploring the evolution and development of secondary sexual trait diversity and sexual dimorphisms. The horns of adult beetles originate during a rapid growth phase during the prepupal stage of larval development, and differential activation of growth during this time is either implicitly or explicitly assumed to be the sole mechanism underlying intra- and interspecific differences in adult horn expression. Here I show that this assumption is not based on developmental reality. Instead, after their initial prepupal growth phase, beetle horns are extensively remodeled during the subsequent pupal stage via sex- and size-dependent resorption of horn tissue. I show that adult sexual dimorphism in four Onthophagus species is shaped partly or entirely by such pupal remodeling rather than by differential growth. Specifically, I show that after a sexually monomorphic growth phase, differential pupal horn resorption can generate both regular and reversed sexual dimorphism. Furthermore, I show that in cases in which initial growth is already dimorphic, pupal horn resorption can both magnify and reverse initial dimorphism resulting from differential growth. Finally, I show that complete resorption of pupal horns in both sexes can remove any trace of horn expression from all resulting adults. In such species, examination of adults only would result in the false conclusion that this species lacks the ability to develop a horn. Instead, such species appear to differ from those with sexually dimorphic adults merely in that they activate pupal horn resorption in both sexes rather than in just one. Combined, these results suggest that pupal remodeling of secondary trait expression is taxonomically widespread, at least among Onthophagus species, and is developmentally extensive and remarkably evolutionarily labile. These results have immediate implications for reconstructing the evolutionary history of horned beetles and the role of developmental processes in guiding evolutionary trajectories. I use these results to revise current understanding of the evolutionary developmental biology of secondary sexual traits in horned beetles in particular and holometabolous insects in general. The results presented here seriously call into question whether descriptions of adult diversity patterns alone suffice for meaningful inferences toward understanding the developmental and evolutionary origin of these patterns. These results illustrate that a lasting integration of development into an evolutionary framework must integrate development as a process rather than define it solely by some of its products.

Animal Structures↗

PubMed2006

Conservation, innovation, and the evolution of horned beetle diversity.

Beetle horns represent an evolutionary novelty exhibiting remarkable diversity above and below the species level. Here, we show that four typical appendage patterning genes, extradenticle (exd), homothorax (hth), dachshund (dac), and Distal-less (Dll) are expressed in the context of the development of sexually dimorphic thoracic horns in three Onthophagus species. At least two of these genes, Dll and hth, exhibited expression patterns consistent with a conservation of patterning function during horn development relative to their known roles in the development of insect legs. exd, hth, and dac expression patterns during horn development were largely invariable across species or sexes within species. In contrast, Dll expression was far more discrete and exhibited consistent differences between sexes and species. Most importantly, differences in location and domain size of Dll expression tightly correlated with the degree to which prepupal horn primordia were retained or resorbed before the final adult molt. Our results lend further support to the hypothesis that the origin of beetle horns relied, at least in part, on the redeployment of already existing developmental mechanisms, such as appendage patterning processes and that changes in the exact location and domain size of Dll expression may represent important modifier mechanisms that modulate horn expression in different species or sexes. If correct, this would imply that certain components of genetic basis of horn development may be able to diversify rapidly within lineages and largely independent of phylogenetic distance. We present a first model that integrates presently available data on the genetic regulation of horn development and diversity.

Amino Acid Sequence↗

PubMed2006

A matter of measurements: challenges and approaches in the comparative analysis of static allometries.

Comparisons of static allometries are frequently used to gain insights into patterns and processes underlying morphological and developmental evolution. A study by J. L. Tomkins and coworkers, recently published in the American Naturalist, examined complex nonlinear allometries in three insect species in which males are dimorphic in the expression of secondary sexual traits. Employing a novel approach to analyzing male allometries in these organisms, the authors were able to show that developmental reprogramming of trait primordia is not necessary to explain allometric scaling in two of the species examined, contrary to several previous studies on the same species. Instead, male dimorphisms could be explained by simple exponential growth, an important result that carries with it major evolutionary and developmental implications. Using this study as an example, I highlight some of the methodological challenges involved in analyzing and comparing static allometries and in inferring the developmental processes that underlie them. I end by discussing how correct application of hypothesis testing, on one side, and basic anatomy and developmental biology, on the other, should guide how morphology is measured.

Anatomy↗

PubMed2004

Trade-offs during the development of primary and secondary sexual traits in a horned beetle.

Resource allocation trade-offs during development affect the final sizes of adult structures and have the potential to constrain the types and magnitude of evolutionary change that developmental processes can accommodate. Such trade-offs can arise when two or more body parts compete for a limited pool of resources to sustain their growth and differentiation. Recent studies on several holometabolous insects suggest that resource allocation trade-offs may be most pronounced in tissues that grow physically close to each other. Here we examine the nature and magnitude of developmental trade-offs between two very distant body parts: head horns and genitalia of males of the horned scarab beetle Onthophagus taurus. Both structures develop from imaginal disklike tissues that undergo explosive growth during late larval development but differ in exactly when they initiate their growth. We experimentally ablated the precursor cells that normally give rise to male genitalia at several time points during late larval development and examined the degree of horn development in these males compared to that of untreated and sham-operated control males. We found that experimental males developed disproportionately larger horns. Horn overexpression was weakest in response to early ablation and most pronounced in males whose genital disks were ablated just before larvae entered the prepupal stage. Our results suggest that even distant body parts may rely on a common resource pool to sustain their growth and that the relative timing of growth may play an important role in determining whether, and how severely, growing organs will affect each other during development. We use our findings to discuss the physiological causes and evolutionary consequences of resource allocation trade-offs.

Animals↗

PubMedDate not supplied

Developmental mechanisms of threshold evolution in a polyphenic beetle.

Polyphenic development is thought to play a pivotal role in the origin of morphological novelties. However, little is known about how polyphenisms evolve in natural populations, the developmental mechanisms that may mediate such evolution, and the consequences of such modification for patterns of morphological variation. Here we examine the developmental mechanisms of polyphenism evolution in highly divergent natural populations of the dung beetle, Onthophagus taurus. Males of this species express two alternative morphologies in response to larval feeding conditions. Favorable conditions cause males to grow larger than a threshold body size and to develop a pair of horns on their heads. Males that encounter relatively poor conditions during larval life do not reach this threshold size and remain hornless. Exotic populations of O. taurus have diverged dramatically in body size thresholds in less than 40 years since introduction to new habitats, resulting in the expression of highly divergent and novel horn length-body size scaling relationships in these populations. Here we show that larvae of populations that have evolved a larger threshold body size (1) have to accumulate greater mass to become competent to express the horned morph, (2) require more time to complete the final instar, (3) are less sensitive to the juvenile hormone (JH) analogue methoprene, and (4) exhibit a delay in the sensitive period for methoprene relative to other developmental events. JH has been shown previously to control horn expression in this species. Our results show that threshold evolution may be mediated via changes in the degree and timing of sensitivity to JH and may result in correlated changes in the dynamics and duration of larval development. Strain-specific differences in JH sensitivity have previously been demonstrated in other insects. However, to the best of our knowledge this is the first demonstration that changes in the timing of the sensitive period for JH may play an equally important role in the evolution of novel thresholds. We discuss our findings in the context of the developmental regulatory mechanisms that underlie polyphenic development and use our results to explore the consequences of, and constraints on, polyphenism evolution in nature.

Animals↗

PubMedDate not supplied

Rapid evolution of a polyphenic threshold.

Polyphenisms are thought to play an important role in the evolution of phenotypic diversity and the origin of morphological and behavioral novelties. However, the extent to which polyphenic developmental mechanisms evolve in natural populations is unknown. Here we contrast patterns of male phenotype expression in native and exotic and ancestral and descendant populations of the horn polyphenic beetle, Onthophagus taurus. Males in this species express two alternative morphologies in response to larval feeding conditions. Favorable conditions cause males to grow larger than a threshold body size and to develop a pair of horns on their heads. Males that encounter relatively poor conditions do not reach this threshold size and remain hornless. We show that exotic and native populations of O. taurus differ significantly in the body size threshold that separates alternative male phenotypes. Comparison with archival museum collections and additional samples obtained from the native range of O. taurus suggests that allometric differences between exotic and native populations do not reflect preexisting variation in the native range of this species. Instead, our data suggest that threshold divergences between exotic and native populations have evolved in less than 40 years since the introduction to a new habitat and have proceeded in opposite directions in two exotic ranges of this species. Finally, we show that the kind and magnitude of threshold divergence between native and exotic populations are similar to differences normally observed between species. Our results support the view that certain components of the developmental control mechanism that underlie polyphenic development can evolve rapidly in natural populations and may provide important avenues for phenotypic differentiation and diversification in nature. We discuss the role of developmental control mechanisms in the origin of allometric diversification and explore potential evolutionary mechanisms that could drive scaling relationship evolution in nature.

Adaptation, Biological↗

PubMedDate not supplied

Diverse developmental mechanisms contribute to different levels of diversity in horned beetles.

An ongoing challenge to evolutionary developmental biology is to understand how developmental evolution on the level of populations and closely related species relates to macroevolutionary transformations and the origin of morphological novelties. Here we explore the developmental basis of beetle horns, a morphological novelty that exhibits remarkable diversity on a variety of levels. In this study, we examined two congeneric Onthophagus species in which males develop into alternative horned and hornless morphs and different sexes express marked sexual dimorphism. In addition, both species differ in the body region (head vs. thorax) that develops the horn. Using a comparative morphological approach we show that prepupal growth of horn primordia during late larval development, as well as reabsorption of horn primordia during the pupal stage, contribute to horn expression in adults. We also show that variable combinations of both mechanisms are employed during development to modify horn expression of different horns in the same individual, the same horn in different sexes, and different horns in different species. We then examine expression patterns of two transcription factors, Distal-less (Dll) and aristaless (al), in the context of prepupal horn growth in alternative male morphs and sexual dimorphisms in the same two species. Expression patterns are qualitatively consistent with the hypothesis that both transcription factors function in the context of horn development similar to their known roles in patterning a wide variety of arthropod appendages. Our results suggest that the origin of morphological novelties, such as beetle horns, rests, at least in part, on the redeployment of already existing developmental mechanisms, such as appendage patterning processes. Our results also suggest, however, that little to no phylogenetic distance is needed for the evolution of very different modifier mechanisms that allow for substantial modulation of trait expression at different time points during development in different species, sexes, or tissue regions of the same individual. We discuss the implications of our results for our understanding of the evolution of horned beetle diversity and the origin and diversification of morphological novelties.

Animals↗