Gene expression suggests decoupled dorsal and ventral segmentation in the millipede Glomeris marginata (Myriapoda: Diplopoda)

Diplopods (millipedes) are known for their irregular body segmentation. Most importantly, the number of dorsal segmental cuticular plates (tergites) does not match the number of ventral structures (e.g., sternites). Controversial theories exist to explain the origin of this so-called diplosegmentation. We have studied the embryology of a representative diplopod, Glomeris marginata, and have analyzed the segmentation genes engrailed (en), hedgehog (hh), cubitus-interruptus (ci), and wingless (wg). We show that dorsal segments can be distinguished from ventral segments. They differ not only in number and developmental history, but also in gene expression patterns. engrailed, hedgehog, and cubitus-interruptus are expressed in both ventral and dorsal segments, but at different intrasegmental locations, whereas wingless is expressed only in the ventral segments, but not in the dorsal segments. Ventrally, the patterns are similar to what has been described from Drosophila and other arthropods, consistent with a conserved role of these genes in establishing parasegment boundaries. On the dorsal side, however, the gene expression patterns are different and inconsistent with a role in boundary formation between segments, but they suggest that these genes might function to establish the tergite borders. Our data suggest a profound and rather complete decoupling of dorsal and ventral segmentation leading to the dorsoventral discrepancies in the number of segmental elements. Based on gene expression, we propose a model that may resolve the hitherto controversial issue of the correlation between dorsal tergites and ventral leg pairs in basal diplopods (e.g., Glomeris) and is suggestive also for derived, ring-forming diplopods (e.g., Juliformia).     

MODULARITY AND SCALING IN FAST MOVEMENTS: POWER AMPLIFICATION IN MANTIS SHRIMP

Extremely fast animal actions are accomplished with mechanisms that reduce the duration of movement. This process is known as power amplification. Although many studies have examined the morphology and performance of power‐amplified systems, little is known about their development and evolution. Here, we examine scaling and modularity in the powerful predatory appendages of a mantis shrimp, Gonodactylaceus falcatus (Crustacea, Stomatopoda). We propose that power‐amplified systems can be divided into three units: an engine (e.g., muscle), an amplifier (e.g., spring), and a tool (e.g., hammer). We tested whether these units are developmentally independent using geometric morphometric techniques that quantitatively compare shapes. Additionally, we tested whether shape and several mechanical features are correlated with size and sex. We found that the morphological regions that represent the engine, amplifier, and tool belong to independent developmental modules. In both sexes, body size was positively correlated with the size of each region. Shape, however, changed allometrically with appendage size only in the amplifier (both sexes) and tool (males). These morphological changes were correlated with strike force and spring force (amplifier), but not spring stiffness (amplifier). Overall, the results indicate that each functional unit belongs to different developmental modules in a power‐amplified system, potentially allowing independent evolution of the engine, amplifier, and tool.     

Sexual size dimorphism and assortative mating in Carolina Wrens

ABSTRACT.   Sexual size dimorphism (SSD) may be due to sexual and natural selection, but identifying specific mechanisms that generate such dimorphism in a species is difficult. I examined SSD in Carolina Wrens ( Thryothorus ludovicianus ) by examining (1) the degree of SSD in the population and between pairs using five morphometrics, (2) assortative mating patterns based on size and age, and (3) relationships between size and longevity. Analysis revealed that males were significantly larger than females in all body measurements. For example, mass, bill, and wing measurements yielded a canonical variable that permitted separation of the sexes and linear classification functions correctly determined the sex of 95% (238/250) of all wrens measured. No evidence was found to suggest that SSD was related to resource partitioning. However, assortative mating trends based on morphometrics (e.g., wing length), positive associations between longevity and morphometrics (e.g., wing length in females and body size in males), and intense male-male contests for territorial resources year-round provide evidence that sexual selection may contribute to SSD in Carolina Wrens.     

Maternal body size as an evolutionary constraint on egg size in a butterfly

Genetic and developmental constraints have often been invoked to explain patterns of existing morphologies. Yet, empirical tests addressing this issue directly are still scarce. We here set out to investigate the importance of maternal body size as an evolutionary constraint on egg size in the tropical butterfly Bicyclus anynana, employing an artificial two-trait selection experiment on simultaneous changes in body and egg size (synergistic and antagonistic selection). Selection on maternal body size and egg size was successful in both the synergistic and the antagonistic selection direction. Yet, responses to selection and realized heritabilities varied across selection regimes: the most extreme values for pupal mass were found in the synergistic selection directions, whereas in the antagonistic selection direction realized heritabilities were low and nonsignificant in three of four cases. In contrast, for egg size the highest values were obtained in the lines selected for low pupal mass. Thus, selection on body size yielded a stronger correlated response in egg size than vice versa, which is likely to bias (i.e., constrain), if weakly, evolutionary change in body size. However, it seems questionable whether this will prevent evolution toward novel phenotypes, given enough time and that natural selection is strong. Correlated responses to selection were overall weak. Egg and larval development times tended to be associated with changes in maternal size, whereas variation in pupal development times weakly tended to follow variation in egg size. Lifetime fecundity was similar across selection regimes, except for females simultaneously selected for large body mass and small egg size, exhibiting increased fecundity. Multiple regressions showed that lifetime fecundity and concomitantly reproductive investment were primarily determined by longevity, as expected for an income breeder, whereas egg size was primarily determined by pupal mass. Evidence for a phenotypic trade-off between egg size and number was weak.     

Cellular consequences in the brain and liver of age-specific selection for rate of development in mice

Changes in cell number (hyperplasia) and cell size (hypertrophy) in the brain and liver are described for mice subjected to 24 generations of age-specific restricted index selection for rate of development in body weight. One selection treatment (E) altered rate of development between birth and 10 days of age, another treatment (L) involved changes in rate of development between 28 and 56 days of age, while a third control treatment (C) involved random selection. Each selection treatment was replicated three times. These age-specific selection treatments focused on intervals during ontogeny when different developmental processes (hypertrophy or hyperplasia) were more predominant in the control of growth. Significant changes in brain and liver weight occurred at both 28 and 70 days of age. Early selection (E) generated significant changes in the number of cells in the brain while later selection (L) had no effect since the brain had stopped growth before selection was initiated. For the liver, early and late selection produced significant effects on both cell number and cell size. These results describe the dynamic and multidimensional aspects of selection in terms of its ability to alter different cellular and developmental components of complex morphological traits.     

A machine‐learning approach for extending classical wildlife resource selection analyses

Resource selection functions (RSFs) are tremendously valuable for ecologists and resource managers because they quantify spatial patterns in resource utilization by wildlife, thereby facilitating identification of critical habitat areas and characterizing specific habitat features that are selected or avoided. RSFs discriminate between known‐use resource units (e.g., telemetry locations) and available (or randomly selected) resource units based on an array of environmental features, and in their standard form are performed using logistic regression. As generalized linear models, standard RSFs have some notable limitations, such as difficulties in accommodating nonlinear (e.g., humped or threshold) relationships and complex interactions. Increasingly, ecologists are using flexible machine‐learning methods (e.g., random forests, neural networks) to overcome these limitations. Herein, we investigate the seasonal resource selection patterns of mule deer (Odocoileus hemionus) by comparing a logistic regression framework with random forest (RF), a popular machine‐learning algorithm. Random forest (RF) models detected nonlinear relationships (e.g., optimal ranges for slope and elevation) and complex interactions which would have been very challenging to discover and characterize using standard model‐based approaches. Compared with standard RSF models, RF models exhibited improved predictive skill, provided novel insights about resource selection patterns of mule deer, and, when projected across a relevant geographic space, manifested notable differences in predicted habitat suitability. We recommend that wildlife researchers harness the strengths of machine‐learning tools like RF in addition to “classical” tools (e.g., mixed‐effects logistic regression) for evaluating resource selection, especially in cases where extensive telemetry data sets are available.     

Do large dogs die young?

In most animal taxa, longevity increases with body size across species, as predicted by the oxidative stress theory of aging. In contrast, in within-species comparisons of mammals and especially domestic dogs (e.g. Patronek et al., '97; Michell, '99; Egenvall et al., 2000; Speakman et al., 2003), longevity decreases with body size.We explore two datasets for dogs and find support for a negative relationship between size and longevity if we consider variation across breeds. Within breeds, however, the relationship is not negative and is slightly, but significantly, positive in the larger of the two datasets. The negative across-breed relationship is probably the consequence of short life spans in large breeds. Artificial selection for extremely high growth rates in large breeds appears to have led to developmental diseases that seriously diminish longevity.     

Plasticity of size and growth in fluctuating thermal environments: comparing reaction norms and performance curves

Ectothermic animals exhibit two distinct kinds of plasticityin response to temperature: Thermal performance curves (TPCs),in which an individual's performance (e.g., growth rate) variesin response to current temperature; and developmental reactionnorms (DRNs), in which the trait value (e.g., adult body sizeor development time) of a genotype varies in response to developmentaltemperatures experienced over some time period during development.Here we explore patterns of genetic variation and selectionon TPCs and DRNs for insects in fluctuating thermal environments.First, we describe two statistical methods for partitioningtotal genetic variation into variation for overall size or performanceand variation in plasticity, and apply these methods to availabledatasets on DRNs and TPCs for insect growth and size. Our resultsindicate that for the datasets we considered, genetic variationin plasticity represents a larger proportion of the total geneticvariation in TPCs compared to DRNs, for the available datasets.Simulations suggest that estimates of the genetic variationin plasticity are strongly affected by the number and rangeof temperatures considered, and by the degree of nonlinearityin the TPC or DRN. Second, we review a recent analysis of fieldselection studies which indicates that directional selectionfavoring increased overall size is common in many systems—thatbigger is frequently fitter. Third, we use a recent theoreticalmodel to examine how selection on thermal performance curvesrelates to environmental temperatures during selection. Themodel predicts that if selection acts primarily on adult sizeor development time, then selection on thermal performance curvesfor larval growth or development rates is directly related tothe frequency distribution of temperatures experienced duringlarval development. Using data on caterpillar temperatures inthe field, we show that the strength of directional selectionon growth rate is predicted to be greater at the modal (mostfrequent) temperatures, not at the mean temperature or at temperaturesat which growth rate is maximized. Our results illustrate someof the differences in genetic architecture and patterns of selectionbetween thermal performance curves and developmental reactionnorms.     

Selection on an extreme weapon in the frog‐legged leaf beetle (Sagra femorata)

Biologists have been fascinated with the extreme products of sexual selection for decades. However, relatively few studies have characterized patterns of selection acting on ornaments and weapons in the wild. Here, we measure selection on a wild population of weapon‐bearing beetles (frog‐legged leaf beetles: Sagra femorata) for two consecutive breeding seasons. We consider variation in both weapon size (hind leg length) and in relative weapon size (deviations from the population average scaling relationship between hind leg length and body size), and provide evidence for directional selection on weapon size per se and stabilizing selection on a particular scaling relationship in this population. We suggest that whenever growth in body size is sensitive to external circumstance such as nutrition, then considering deviations from population‐level scaling relationships will better reflect patterns of selection relevant to evolution of the ornament or weapon than will variation in trait size per se. This is because trait‐size versus body‐size scaling relationships approximate underlying developmental reaction norms relating trait growth with body condition in these species. Heightened condition‐sensitive expression is a hallmark of the exaggerated ornaments and weapons favored by sexual selection, yet this plasticity is rarely reflected in the way we think about—and measure—selection acting on these structures in the wild.     

Individual-level selection as a cause of Cope's rule of phyletic size increase

Cope's rule, the tendency for species within a lineage to evolve towards larger body size, has been widely reported in the fossil record, but the mechanisms leading to such phyletic size increase remain unclear. Here we show that selection acting on individual organisms generally favors larger body size. We performed an analysis of the strength of directional selection on size compared with other quantitative traits by evaluating 854 selection estimates from 42 studies of contemporaneous natural populations. For size, more than 79% of selection estimates exceed zero, whereas for other morphological traits positive and negative values are similar in frequency. The selective advantage of increased size occurs for traits implicated in both natural selection (e.g., differences in survival) and sexual selection (e.g., differences in mating success). The predominance of positive directional selection on size within populations could translate into a macroevolutionary trend toward increased size and thereby explain Cope's rule.     

Reproductive versus ecological advantages to larger body size in female snakes, Vipera aspis

Body size can influence an organism's microevolutionary fitness either via ecological factors (ecological selection) or changes in reproductive output (sexual or fecundity selection). Published studies on sexual dimorphism in reptiles have generally focussed on sexual-selective forces on males, under the implicit assumption that the intensity of fecundity selection in females (and hence, overall selection on female body size) is likely to be relatively consistent among lineages. In this paper, we explore the degree to which larger body size enhances ecological attributes (e.g., food intake, growth, survival) and reproductive output (reproductive frequency, litter size, offspring size, offspring viability) in free-ranging female aspic vipers, Vipera aspis . The less-than-annual reproductive frequency of these animals allows us to make a direct comparison between females in years during which they concentrate on "ecological" challenges (especially building energy reserves) versus reproductive challenges (producing a litter). Because female snakes have limited abdominal space to hold the clutch (litter), we expect that fecundity should depend on body size. However, our data show that larger body size had a more consistent effect on ecological attributes (such as feeding rates and "costs of reproduction") than on reproductive output per se. Indeed, total reproductive output was maximised at intermediate body sizes. These results suggest that variation in female body size among and within species (and hence, in the degree of sexual dimorphism) may be driven by the ecological as well as reproductive consequences of body size variation in both sexes.     

Ecological and developmental context of natural selection: maternal effects and thermally induced plasticity in the frog Bombina orientalis

Variation in fitness generated by differences in functional performance can often be traced to morphological variation among individuals within natural populations. However, morphological variation itself is strongly influenced by environmental factors (e.g., temperature) and maternal effects (e.g., variation in egg size). Understanding the full ecological context of individual variation and natural selection therefore requires an integrated view of how the interaction between the environment and development structures differences in morphology, performance, and fitness. Here we use naturally occurring environmental and maternal variation in the frog Bombina orientalis in South Korea to show that ovum size, average temperature, and variance in temperature during the early developmental period affect body sizes, shapes, locomotor performance, and ultimately the probability of an individual surviving interspecific predation in predictable but nonadditive ways. Specifically, environmental variability can significantly change the relationship between maternal investment in offspring and offspring fitness so that increased maternal investment can actually negatively affect offspring over a broad range of environments. Integrating environmental variation and developmental processes into traditional approaches of studying phenotypic variation and natural selection is likely to provide a more complete picture of the ecological context of evolutionary change.     

Early Rearing Conditions Affect the Development of Body Size and Song in Bengalese Finches

Birdsong is an acoustic ornament. According to indicator models, a trait must be costly to act as an honest signal, but the potential costs of elaborate songs are still poorly understood. The developmental stress hypothesis suggests that learned song characteristics could be an honest indicator of early developmental conditions because the brain structures associated with learning songs are susceptible to early developmental stress, which could thus affect song development. Unlike previous studies of developmental stress that examined the effect of a stress hormone or restricted nutrition, we observed Bengalese finches under semi‐natural breeding conditions in captivity to investigate the relationship between early rearing conditions (e.g., brood size and sex ratio) and the subsequent variation in body size and song among individuals. Our results suggest that the early rearing environment directly affects body size and song complexity, whereas song output is determined mainly by body size. These results support the developmental stress hypothesis. Moreover, our findings are the first to show that developmental condition affects not only the number of note types but also the syntactical complexity of the song.     

Cell lineage dependent and independent control of Purkinje cell number in the mammalian CNS: further quantitative studies of lurcher chimeric mice

Recent quantitative studies of lurcher chimeric mice have shown that the adult population of cerebellar Purkinje cells can properly be described as a small number of developmental clones of cells. The clones are not seen as patches of contiguous neurons; rather, the cells of any one clone distribute throughout the half-cerebellum that contains them, intermingling extensively with the Purkinje cells of other linkages. Lurcher----wild-type chimeras were analyzed using the cell autonomous Purkinje-cell-lethal mutant, lurcher (+/Lc), as a cell marker. Cell counts from these chimeras revealed that the number of surviving Purkinje cells was always an integral multiple of a unit clone size. These numerical quanta are the evidence for the existence of Purkinje cell developmental clones. When two different inbred strains of mouse were compared (C3H/HeJ and C57BL/6), the resulting clonal analysis showed that the unit clone size (i.e., the number of Purkinje cells in one quantum) is an autonomous property of the lineage and hence, presumably, intrinsic to the progenitor cell that founded it. The current study uses the lurcher chimeric mouse system to examine the cell lineage relationships among the Purkinje cells of a third inbred strain of mouse, AKR/J. The data both support and extend our previous studies. Quantitative analysis reveals that the Purkinje cells of this strain also exist in clones, and the size of these clones is also strain-specific. The number of cells in a single clone (7850), however, is different from either C3H/HeJ (10,200) or C57BL/6 (9200). The fact that this value is so highly polymorphic among the inbred strains of mouse makes it likely that, rather than being a function of different alleles at a single genetic locus, clone size may well represent a multifactorial (but still cell-autonomous) property of developing Purkinje cells. Additional results from a single chimeric animal suggest strongly that clone number (i.e., the number of progenitors selected to found the population) is not strain-specific but results instead from cell:cell interactions during early nervous system formation.     

DEVELOPMENT OF FLOWER FORM IN AN ALLOTETRAPLOID CLARKIA AND ITS PARENTAL DIPLOID SPECIES

The allotetraploid Clarkia delicata possesses a floral phenotype and breeding system intermediate to its diploid progenitors. Three patterns were observed in a comparative study of anther, sepal, and petal development using allometry and scanning electron micrographs. In Pattern 1 (e.g., anther), all three species are similar at inception and in subsequent development. Anthers of the allotetraploid mature at a size intermediate to both diploids. In Pattern 2 (e.g., sepal and petal limb), diploids exhibit divergent developmental patterns, and the allotetraploid develops similarly to one diploid. In Pattern 3 (e.g., petal size and shape), diploids exhibit divergent developmental patterns, and the allotetraploid is variously intermediate to both. In petal size (length vs. width), the diploid developmental pathways are parallel, and the allotetraploid is intermediate at all points of development. In petal shape (limb length above widest point/length below widest point vs. petal width), diploid developmental pathways intersect, and the allotetraploid is similar to one diploid at inception and the other in subsequent development.     

Adaptation and constraint in the evolution of Drosophila melanogaster wing shape

SUMMARY We have taken advantage of parallel instances of natural selection on body size in Drosophila melanogaster to investigate constraints and adaptation affecting wing shape. Using recently developed techniques for statistical shape analysis, we have examined variation in wing shape in similar body size clines on three continents. Gender-related shape differences were constant among all populations, suggesting that gender differences represent a developmental constraint on wing shape. In contrast, the underlying shape varied significantly between continents and shape change within each cline (i.e., between small and large body size populations) also varied between continents. Therefore, variation at these two levels presumably results from either drift or natural selection. Functional considerations suggest that shape variation between the continents is unlikely to be adaptive. However, cline-related shape change, which we show has a significant allometric component, may be adaptive. The overall range of wing shape variation, across a large range of wing size, is extremely small, and the possibility that wing shape is subject to stabilizing selection (or canalization) is discussed.     

Temporal and spatial complexity of maternal thermoregulation in tropical pythons

Parental care is a widespread adaptation that evolved independently in a broad range of taxa. Although the dynamics by which two parents meet the developmental needs of offspring are well studied in birds, we lack understanding about the temporal and spatial complexity of parental care in taxa exhibiting female-only care, the predominant mode of parental care. Thus, we examined the behavioral and physiological mechanisms by which female water pythons Liasis fuscus meet a widespread developmental need (thermoregulation) in a natural setting. Although female L. fuscus were not facultatively thermogenic, they did use behaviors on multiple spatial scales (e.g., shifts in egg-brooding postures and surface activity patterns) to balance the thermal needs of their offspring throughout reproduction (gravidity and egg brooding). Maternal behaviors in L. fuscus varied by stage within reproduction and were mediated by interindividual variation in body size and fecundity. Female pythons with relatively larger clutch sizes were cooler during egg brooding, suggesting a trade-off between reproductive quantity (size of clutch) and quality (developmental temperature). In nature, caregiving parents of all taxa must navigate both extrinsic factors (temporal and spatial complexity) and intrinsic factors (body size and fecundity) to meet the needs of their offspring. Our study used a comprehensive approach that can be used as a general template for future research examining the dynamics by which parents meet other developmental needs (e.g., predation risk or energy balance).     

The role of olfaction throughout juvenile development: Functional adaptations in elasmobranchs

Seven elasmobranch species, a group known for their highly‐developed sense of smell, were examined for developmental changes in the number of olfactory lamellae, the size of the surface area of the sensory olfactory epithelium and the mass of both the olfactory rosettes (primary input to the CNS), and the olfactory bulbs. Within each species, juveniles possessed miniature versions of the adult olfactory organs, visually not distinguishable from these and without any obvious structural differences (e.g., with respect to the number of lamellae and the extent of secondary folding) between differently sized individuals. The size of the olfactory organs was positively correlated with body length and body mass, although few species showed proportional size scaling. In Aetobatus narinari and Aptychotrema rostrata, olfactory structures increased in proportion to body size. With respect to the growth of the olfactory bulb, all species showed allometric but not proportional growth. Olfaction may be of particular importance to juveniles in general, which are often subjected to heavy predation rates and fierce inter/intraspecific competition. Accordingly, it would be advantageous to possess a fully functional olfactory system early on in development. Slow growth rates of olfactory structures could then be attributed to a greater reliance on other sensory systems with increasing age or simply be regarded as maintaining an already optimized olfactory system. J. Morphol., 2010. © 2009 Wiley‐Liss, Inc.     

Incorporating an ontogenetic perspective into evolutionary theory of sexual size dimorphism

Sexual size dimorphism (SSD) describes divergent body sizes of adult males and females. While SSD has traditionally been explained by sexual and fecundity selection, recent advances in physiology and developmental biology emphasize that SSD would occur proximately because of sexual differences in ontogenetic growth trajectories (i.e., growth rate and duration). Notably, these ontogenetic traits are subject to energetic or time constraints and thus traded off with fitness components (e.g., survival and reproduction). To elucidate the importance of such ontogenetic trade‐offs in the evolution of SSD, we developed a new theoretical framework by extending quantitative genetic models for the evolution of sexual dimorphism in which we reinterpret the trait as body size and reformulate sex‐specific fitness in size‐dependent manners. More specifically, we assume that higher growth rate or longer growth duration leads to larger body size and higher reproductive success but incurs the cost of lower survivorship or shorter reproduction period. We illustrate how two sexes would optimize ontogenetic growth trajectories in sex‐specific ways and exhibit divergent body sizes. The present framework provides new insights into the evolutionary theory of SSD and predictions for empirical testing.     

Autonomous puffing patterns in thoracic and abdominal polytene bristle cell chromosomes of the flesh fly Sarcophaga barbata

The puffing patterns of the thoracic and abdominal polytene bristle cell chromosomes were investigated in Sarcophaga barbata during a 10-day period of pupal development. The autonomous differentiation of imaginal disk descendants is visualized microscopically at the chromosomal level by the cell autonomous puff activities of the polytene bristle cell chromosomes. The sequence of chromosomal activities is strictly stage specific in both cell types. The changes in the puffing pattern are closely corelated with development. The puffing pattern changes synchronously in all bristle cells of a certain body region, e.g., the scutellum or the fifth abdominal tergit. However, there is no synchrony between the puffing pattern changes of the thoracic and abdominal bristle cells. The loci of the abdominal bristle cells are activated one day later than those of the thoracic cells. Each particular puffing pattern truly represents a particular developmental state of the bristle, regardless of body location. That is, the bristle cell chromosomes of various body segments control the timing of their puffing activities autonomously and puff formation and puff regression are not hormonally synchronized.