The behavioral ecology of threshold evolution in a polyphenic beetle

Facultative expression of alternative male morphologies is thoughtto allow individual males to select the phenotype with the highestfitness gain given their competitive status relative to othermales with which they compete for females. Choice of, or switchingbetween, morphs commonly relies on developmental threshold responses.Evolutionary changes in developmental threshold responses arethought to provide an important avenue for phenotypic diversificationand the evolution of morphological and behavioral novelties.However, the extent to which alternative male phenotypes andtheir underlying threshold responses actually evolve in naturalpopulations is unclear. Likewise, the ecological factors thatshape the evolution of threshold responses in natural populationsare unexplored for most organisms, as are the consequences ofsuch modifications for patterns of morphological diversity.I examined the ecological basis of rapid threshold evolutionin exotic populations of the horn-polyphenic dung beetle Onthophagustaurus. Male O. taurus vary continuously in body size as a functionof larval feeding conditions. Only males that exceed a criticalthreshold body size develop a pair of long horns on their heads,whereas males below this threshold remain hornless. Populationsin two exotic ranges of this species, the eastern United Statesand western Australia, have diverged in the mean threshold bodysize, which has resulted in the evolution of highly divergentand novel horn length–body size allometries in these populations.Populations in a third and previously unstudied exotic rangeof O. taurus in eastern Australia exhibit threshold body sizesroughly intermediate between the eastern U.S. and western Australianpopulations. I tested three hypothesis to explain how differencesin ecological and demographic factors can drive allometric divergencesbetween populations, using data derived from comparative, standardizedsampling of a large number of populations in each exotic range.Results suggest that differences in the intensity of both intra-and interspecific competition have contributed to the evolutionof divergent thresholds in these populations. My results donot support the hypothesis that shifts in threshold body sizesto larger body sizes are a consequence of increases in the meanbody size of competing males. I discuss my results in the contextof Onthophagus mating systems and the evolutionary implicationsof threshold evolution.     

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.     

Allometric plasticity in a polyphenic beetle

Abstract 1. Environmental conditions, such as variation in nutrition, commonly contribute to morphological variation among individuals by affecting body size and the expression of certain morphological traits; however the scaling relationship between a morphological trait and body size over a range of body sizes is generally assumed not to change in response to environmental fluctuation (allometric plasticity), but instead to be constant and diagnostic for a particular trait and species or population. The work reported here examined diet‐induced allometric plasticity in the polyphenic beetle Onthophagus taurus Schreber (1759) (Coleoptera: Scarabaeidae). 2. Male O. taurus vary in body size depending on larval nutrition. Only males above a critical body size threshold express fully developed horns; males smaller than this threshold develop only rudimentary horns or no horns at all. 3. Field populations that naturally utilise two different resources for feeding larvae (horse dung vs. cow manure) exhibited significant differences in the average scaling relationship between body size and male horn length over the same range of body sizes. Males collected from cow manure populations expressed consistently longer horns for a given body size than males collected from horse dung populations. 4. Males reared in the laboratory on horse dung or cow manure also exhibited significant differences in the average scaling relationship between body size and horn length. Differences between laboratory populations reared on horse dung or cow manure were of the same kind and magnitude as differences between field populations that utilise these different resources naturally. 5. These findings suggest that between‐population differences in scaling relationships between horn length and body size can be the product of differences in the quality of resources available to developing larvae. Results are discussed in the context of onthophagine mating systems and recent insights in the developmental and endocrine control of horn polyphenisms.     

Diversification in subtropical mountains: phylogeography, Pleistocene demographic expansion, and evolution of polyphenic mandibles in Taiwanese stag beetle, Lucanus formosanus

Pleistocene glacial oscillations have had profound impacts on the historical population dynamics of extant species. However, the genetic consequences of past climatic changes depend largely on the latitude and topography of the regions in question. This study investigates the effect of Pleistocene glacial periods and the Central Mountain Range on the phylogeography, historical demography, and phenotypic differentiation of a montane forest-dwelling stag beetle, Lucanus formosanus (Coleoptera: Lucanidae), which exhibits extensive mandible variations across mountain ranges in subtropical Taiwan. Analyses of mitochondrial (cox1) and nuclear (wg) loci reveal that L. formosanus originated nearly 1.6 million years ago (Mya) in the early Pleistocene period and consisted of geographically overlapping Alishan and Widespread clades. A drastic population expansion starting approximately 0.2 Mya in the Widespread clade likely resulted from altitudinal range shift of the temperate forests, which was closely tied to the arrival of the Riss glacial period in the late Middle Pleistocene. A ring-like pattern of historical gene flow among neighboring populations in the vicinity of the Central Mountain Range indicates that the mountains constitute a strong vicariant barrier to the east-west gene flow of L. formosanus populations. A geographic cline of decreasing mandible size from central to north and south, and onto southeast of Taiwan is inconsistent with the low overall phylogeographic structures. The degree of mandible variation does not correlate with the expected pattern of neutral evolution, indicating that the evolutionary diversification of this morphological weapon is most likely subject to sexual or natural selection. We hypothesize that the adaptive evolution of mandibles in L. formosanus is shaped largely by the habitat heterogeneity.     

Dual structural color mechanisms in a scarab beetle

The cuticle of a Mycterophallus cetoniine scarab species displays both red iridescence due to a multilayer reflector mechanism and rainbow iridescence due to a superimposed diffraction grating mechanism. This is the first reported example of an animal possessing two independent classes of structural colors arising from interference at the wavelengths of visible light. In this work, the Mycterophallus cuticle is characterized by light microscopy, spectrophotometry, scanning electron microscopy, and transmission electron microscopy. We compare the cuticle of the Mycterophallus species to two closely related Lomaptera scarab species, one with only a multilayer reflector and the second with only a diffraction grating. We calculate the correspondence between the nanostructural parameters and the optical properties of the Mycterophallus cuticle to determine the relative optical contributions of the two color mechanisms and the interactions between them. J. Morphol., 2010. © 2010 Wiley‐Liss, Inc.     

Character displacement in polyphenic tadpoles

Biologists have long known that closely related species are often phenotypically different where they occur together, but are indistinguishable where they occur alone. The causes of such character displacement are controversial, however. We used polyphenic spadefoot toad tadpoles (Spea bombifrons and S. multiplicata) to test the hypothesis that character displacement evolves to minimize competition for food. We also sought to evaluate the role of phenotypic plasticity in the mediation of competitive interactions between these species. Depending on their diet, individuals of both species develop into either a small-headed omnivore morph, which feeds mostly on detritus, or a large-headed carnivore morph, which specializes on shrimp. Laboratory experiments and surveys of natural ponds revealed that the two species were more dissimilar in their tendency to produce carnivores when they occurred together than when they occurred alone. This divergence in carnivore production was expressed as both character displacement (where S. multiplicata's propensity to produce carnivores was lower in sympatry than in allopatry) and as phenotypic plasticity (where S. multiplicata facultatively enhanced carnivore production in S. bombifrons, and S. bombifrons facultatively suppressed carnivore production in S. multiplicata). In separate experiments, we established that S. bombifrons (the species for which carnivore production was enhanced) was the superior competitor for shrimp. Conversely, S. multiplicata (the species for which carnivore production was suppressed and omnivore production enhanced) was the superior competitor for detritus. These results therefore demonstrate that selection to minimize competition for food can cause character displacement. They also suggest that both character displacement and phenotypic plasticity may mediate competitive interactions between species.     

The evolution of beetle pollination in a South African orchid

The pollination biology of the orchid Ceratandra grandiflora was investigated in order to determine whether the partial loss of a specialized floral reward (i.e., oil) was the result of an incomplete shift from one specialized pollinator to another. In the three-species clade of section Ceratandra, there has been a progressive loss of the oil-secreting callus. lt is always present in C atrata, sometimes present in C. grandiflora, and never present in C. globosa. Thirty-nine to 67% of individuals in populations of C. grandiflora bear the callus gland, but gland presence has no signifikant effect on the proportion of flowers pollinated. Pollinator observations show that the shift in pollinators is complete and that the oil-secreting callus is a vestige of the ancestral oil-bee pollination system that no longer plays a role in pollination. C grandiflora is pollinated almost exclusively by a single species of hopliine beetle (Scarabaeidae). Experiments with artificial flower traps indicate that color alone can explain the attraction of beetles to C. grandiflora, despite the absence of a floral reward. The proportion of C. grandiflora flowers pollinated (50.2 and 61.1%; N = 524 and 324 flowers, respectively) is unusually high for a plant that relies on generalized food deception and is probably due to the use of inflorescences as mating sites (i.e., rendezvous pollination).     

Developmental mechanisms in heterospory

The megasporangium of Selaginella sulcata (Desv.) Spring contains approximately equal numbers of megasporocytes of two kinds that can be distinguished on size and ultrastructure. These are called viable and non-viable. During the prophase of meiosis the non-viable megasporocytes degenerate by a process corresponding to cellular autophagy. One viable megasporocyte completes the meiotic cycle and the others persist, presumably as diploid cells, in the post-meiotic megasporangium; and it is shown that in S. plana (Desv.) Hieron an exine is formed on these. The possible significance of the particular disposition of the mitochondria and of intranuclear vesicles in the viable megasporocytes is discussed.     

Facultative paternal investment in the polyphenic beetle Onthophagus taurus: the role of male morphology and social context

Members of a population often differ significantly in theirparental investment. Such variation is generally believed tohave important consequences for mating system evolution andhas been suggested to play an important role in the evolutionof some secondary sexual traits and displays. Recent studiessuggest that individuals are able to adjust the intensity and kindof parental investment they provide according to the breedingconditions they encounter. As a consequence, between-individualvariation in parental investment may depend more on externalconditions than previously thought for these taxa. This mayhave important implications for current perspectives on therole of differential parental investment in the evolution andmaintenance of certain mating systems and sexual selection regimes.Here I quantify patterns of variation in paternal investmentas a function of social conditions in a species of beetle thatis dimorphic for male horn morphology. I demonstrate that undercertain conditions (namely, the absence of other males), paternalassistance covaries with male morphology, with horned males investingsubstantially more time in assisting females than hornless males.I also show that the magnitude of differences in paternal investmentbetween male morphs varies in response to external conditions.In the presence of other males, paternal assistance was negligiblefor both male morphs, who instead invested substantially andequally in mate-securing behaviors. I use my findings to discussthe significance of variation in paternal assistance for onthophaginemating systems and evaluate ideas proposed to explain the evolutionof alternative morphologies in the genus Onthophagus.     

The initiation of metamorphosis as an ancient polyphenic trait and its role in metazoan life-cycle evolution

Comparative genomics of representative basal metazoans leaves little doubt that the most recent common ancestor to all modern metazoans was morphogenetically complex. Here, we support this interpretation by demonstrating that the demosponge Amphimedon queenslandica has a biphasic pelagobenthic life cycle resembling that present in a wide range of bilaterians and anthozoan cnidarians. The A. queenslandica life cycle includes a compulsory planktonic larval phase that can end only once the larva develops competence to respond to benthic signals that induce settlement and metamorphosis. The temporal onset of competence varies between individuals as revealed by idiosyncratic responses to inductive cues. Thus, the biphasic life cycle with a dispersing larval phase of variable length appears to be a metazoan synapomorphy and may be viewed as an ancestral polyphenic trait. Larvae of a particular age that are subjected to an inductive cue either maintain the larval form or metamorphose into the post-larval/juvenile form. Variance in the development of competence dictates that only a subset of a larval cohort will settle and undergo metamorphosis at a given time, which in turn leads to variation in dispersal distance and in location of settlement. Population divergence and allopatric speciation are likely outcomes of this conserved developmental polyphenic trait.     

Developmental mechanisms of gyrification

Folding of the cerebral cortex is a fundamental milestone of mammalian brain evolution associated with dramatic increases in size and complexity. Cortex folding takes place during embryonic and perinatal development and is important to optimize the functional organization and wiring of the brain, while allowing fitting a large cortex in a limited cranial volume. Cortex growth and folding are the result of complex cellular and mechanical processes that involve neural stem progenitor cells and their lineages, the migration and differentiation of neurons, and the genetic programs that regulate and fine-tune these processes. Here, we provide an updated overview of the most significant and recent advances in our understanding of developmental mechanisms regulating cortical gyrification.     

Seasonal selection and resource dynamics in a seasonally polyphenic butterfly

Seasonal polyphenisms are widespread in nature, yet the selective pressures responsible for their evolution remain poorly understood. Previous work has largely focussed either on the developmental regulation of seasonal polyphenisms or putative ‘top‐down’ selective pressures such as predation that may have acted to drive phenotypic divergence. Much less is known about the influence of seasonal variation in resource availability or seasonal selection on optimal resource allocation. We studied seasonal variation in resource availability, uptake and allocation in Araschnia levana L., a butterfly species that exhibits a striking seasonal colour polyphenism consisting of predominantly orange ‘spring form’ adults and black‐and‐white ‘summer form’ adults. ‘Spring form’ individuals develop as larvae in the late summer, enter a pupal diapause in the fall and emerge in the spring, whereas ‘summer form’ individuals develop directly during the summer months. We find evidence for seasonal declines in host plant quality, and we identify similar reductions in resource uptake in late summer, ‘spring form’ larvae. Further, we report shifts in the body composition of diapausing ‘spring form’ pupae consistent with a physiological cost to overwintering. However, these differences do not translate into detectable differences in adult body composition. Instead, we find minor seasonal differences in adult body composition consistent with augmented flight capacity in ‘summer form’ adults. In comparison, we find much stronger signatures of sex‐specific selection on patterns of resource uptake and allocation. Our results indicate that resource dynamics in A. levana are shaped by seasonal fluctuations in host plant nutrition, climatic conditions and intraspecific interactions.     

Some biochemical threshold mechanisms

Certain arrangements of enzymatic (bimolecular) subsystems lead to characteristic threshold-type response. Two simple cases of such systems are studied here in terms of steady state behavior and explicit relationships between system and curve parameters. It is found that the curvature of the threshold curve is directly related to the equivalent Michaelis constant and, in the case of saturated threshold curve, the slope of the curve at the idealized threshold is limited by the ratio of saturation to threshold. This slope may be appreciably increased up to a stepwise response at the threshold if a multisubstrate complex of the enzyme is the only species which affects the enzyme mediated transport.     

Developmental trait evolution in trilobites

We performed a tree-based analysis of trilobite postembryonic development in a sample of 60 species for which quantitative data on segmentation and growth increments between putative successive instars are available, and that spans much of the temporal, phylogenetic, and habitat range of the group. Three developmental traits were investigated: the developmental mode of trunk segmentation, the average per-molt growth rate, and the conformity to a constant per-molt growth rate (Dyar's rule), for which an original metric was devised. Growth rates are within the normal range with respect to other arthropods and show overall conformity to Dyar's rule. Randomization tests indicate statistically significant phylogenetic signal for growth in early juveniles but not in later stages. Among five evolutionary models fit via maximum likelihood, one in which growth rates vary independently among species, analogous to Brownian motion on a star phylogeny, is the best supported in all ontogenetic stages, although a model with a single, stationary peak to which growth rates are attracted also garners nontrivial support. These results are not consistent with unbounded, Brownian-motion-like evolutionary dynamics, but instead suggest the influence of an adaptive zone. Our results suggest that developmental traits in trilobites were relatively labile during evolutionary history.     

Genetic architecture underlying convergent evolution of egg-laying behavior in a seed-feeding beetle

Independent populations subjected to similar environments often exhibit convergent evolution. An unresolved question is the frequency with which such convergence reflects parallel genetic mechanisms. We examined the convergent evolution of egg-laying behavior in the seed-feeding beetle Callosobruchus maculatus. Females avoid ovipositing on seeds bearing conspecific eggs, but the degree of host discrimination varies among geographic populations. In a previous experiment, replicate lines switched from a small host to a large one evolved reduced discrimination after 40 generations. We used line crosses to determine the genetic architecture underlying this rapid response. The most parsimonious genetic models included dominance and/or epistasis for all crosses. The genetic architecture underlying reduced discrimination in two lines was not significantly different from the architecture underlying differences between geographic populations, but the architecture underlying the divergence of a third line differed from all others. We conclude that convergence of this complex trait may in some cases involve parallel genetic mechanisms.