DISSECTING CORRELATED CHARACTERS: ADAPTIVE ASPECTS OF PHENOTYPIC COVARIATION IN MELANIZATION PATTERN OF PIERIS BUTTERFLIES

In this study we address the question of how much of the covariation among phenotypic characters observed in natural populations is adaptive. We examine covariation among a set of phenotypic characters that describe the wing-melanization pattern of Pieris butterflies. Previous functional analyses of thermoregulatory performance allow us to predict a priori whether and how different wing melanic characters should be correlated. We quantify and analyze the variation in the wing-melanization pattern within species for a series of Pieris populations from relatively cool environments in North America and compare these results with the predictions based on our adaptive hypothesis. We consider adaptive covariation both for biogeographic variation among populations and for seasonal polyphenism (phenotypic plasticity) within populations. Our hypothesis correctly predicts many of the qualitative features of covariation in melanization among major regions of the wings, at the level of biogeographic variation among populations, for both males and females of Pieris occidentalis. When within-population variation is considered, agreement with the adaptive predictions varies considerably in different populations for both P. occidentalis and P. napi males and females. Agreement for P. napi, particularly the females, is generally poorer than for P. occidentalis. In both species, there is a consistent difference in melanization pattern between alpine and arctic sites; this difference is discussed in relation to the differences in the radiative environment between these two types of “cold” habitats. Our results suggest that some important aspects of phenotypic correlation among wing melanic characters in Pieris are adaptive. We emphasize the important distinction between covariation and co-occurrence of characters, and we discuss these results in relation to the extensive biogeographic variation and phenotypic plasticity (seasonal polyphenism) in Pieris wing-melanization patterns.     

Drosophila wing modularity revisited through a quantitative genetic approach

To predict the response of complex morphological structures to selection it is necessary to know how the covariation among its different parts is organized. Two key features of covariation are modularity and integration. The Drosophila wing is currently considered a fully integrated structure. Here, we study the patterns of integration of the Drosophila wing and test the hypothesis of the wing being divided into two modules along the proximo‐distal axis, as suggested by developmental, biomechanical, and evolutionary evidence. To achieve these goals we perform a multilevel analysis of covariation combining the techniques of geometric morphometrics and quantitative genetics. Our results indicate that the Drosophila wing is indeed organized into two main modules, the wing base and the wing blade. The patterns of integration and modularity were highly concordant at the phenotypic, genetic, environmental, and developmental levels. Besides, we found that modularity at the developmental level was considerably higher than modularity at other levels, suggesting that in the Drosophila wing direct developmental interactions are major contributors to total phenotypic shape variation. We propose that the precise time at which covariance‐generating developmental processes occur and/or the magnitude of variation that they produce favor proximo‐distal, rather than anterior‐posterior, modularity in the Drosophila wing.     

Estimating genetic and phenotypic diversity in a northern hoverfly reveals lack of heterozygosity correlated with significant fluctuating asymmetry of wing traits

The genetic structure and phenotypic diversity of a population of Cheilosia naruska Haarto and Kerppola, 2007 (Diptera, Syrphidae) from Lapland, Finland, was examined through allozyme electrophoresis and wing morphometrics. The morphological identification of the species was verified molecularly using partial sequences of mitochondrial COI and the nuclear ribosomal ITS2 genes comparing with corresponding sequences of a paratype of the taxon. Based on protein electrophoresis, out of 12 analyzed allozyme loci, only one locus (Me) was found to be polymorphic. The low genetic variability was further evidenced by the absence of heterozygote genotypes. Fluctuating asymmetry was used as a measure of developmental stability. For this we used different wing traits that were estimated using both wing landmark positions and metric traits. Procrustes ANOVA and Canonical variate analysis revealed asymmetry in wing metric and wing shape and size, and within each sex considered separately. Principal component analysis revealed similar multivariate patterns of landmark covariation between within-individual variability (fluctuating asymmetry) and variation among individuals. Finally, the observed association between lack of heterozygosity and high level of asymmetry is discussed in light of conservation.     

Morpho morphometrics: Shared ancestry and selection drive the evolution of wing size and shape in Morpho butterflies

Butterfly wings harbor highly diverse phenotypes and are involved in many functions. Wing size and shape result from interactions between adaptive processes, phylogenetic history, and developmental constraints, which are complex to disentangle. Here, we focus on the genus Morpho (Nymphalidae: Satyrinae, 30 species), which presents a high diversity of sizes, shapes, and color patterns. First, we generate a comprehensive molecular phylogeny of these 30 species. Next, using 911 collection specimens, we quantify the variation of wing size and shape across species, to assess the importance of shared ancestry, microhabitat use, and sexual selection in the evolution of the wings. While accounting for phylogenetic and allometric effects, we detect a significant difference in wing shape but not size among microhabitats. Fore and hindwings covary at the individual and species levels, and the covariation differs among microhabitats. However, the microhabitat structure in covariation disappears when phylogenetic relationships are taken into account. Our results demonstrate that microhabitat has driven wing shape evolution, although it has not strongly affected forewing and hindwing integration. We also found that sexual dimorphism of forewing shape and color pattern are coupled, suggesting a common selective force.     

ONTOGENETIC VARIATION IN PATTERNS OF DEVELOPMENTAL AND FUNCTIONAL INTEGRATION IN SKULLS OF SIGMODON FULVIVENTER

Patterns of variation and covariation within populations can influence how characters respond to natural selection and random genetic drift and so constrain the ability of natural selection to modify the phenotype. We examined several potential developmental and functional explanations of character covariation throughout ontogeny using known-age samples of the cotton rat (Sigmodon fulviventer) to identify the causes of covariation and to assess the variability of patterns of covariation throughout postnatal growth. Competing developmental and functional models were fit to samples of orofacial and neurocranial measures by confirmatory factor analysis and evaluated for their ability to reconstruct observed variance-covariance matrices. Samples of successive ages were simultaneously fit to a common model to test the hypothesis that the patterns of developmental and functional integration were invariant between ages. Orofacial characters derived from the same branchial-arch primordium covary early in ontogeny. Subsequently, there is a repatterning of integration that may reflect a transition from developmental to functional sources of integration. Neurocranial characters exhibit even more variation in patterns of covariation: initially, characters appear to comprise a single integrated unit; before puberty, they appear to respond to localized bone growth; after puberty, they form separate calvarial and basicranial components. This ontogenetic variation in patterns of covariation suggests that developmental constraints are transient and flexible and that the consequences of selection may depend upon the age at which it acts.     

A COMPARISON OF TEMPERATURE-INDUCED POLYPHENISM IN AFRICAN BICYCLUS BUTTERFLIES FROM A SEASONAL SAVANNAH-RAINFOREST ECOTONE

Temperature-induced variation and norms of reaction have been analyzed for wing pattern elements of six species belonging to the African butterfly genus Bicyclus (Lepidoptera, Nymphalidae, Satyrinae). Five of these species are sympatric in Malawi and exhibit seasonal polyphenism in the savannah-rainforest ecotone. The sixth species originated from Cameroonian equatorial rainforest. The organisms were laboratory reared under four different temperature conditions ranging from 17–28°C. The variation in response to temperature is described by principal component analysis (PCA). Discrimination on the basis of plastic wing pattern characters was performed by discriminant function analysis (DFA) and unweighed pair-group method algorithm (UPGMA) clustering. A phylogenetic reconstruction based on adaptive plastic wing characters was compared with a cladogram built on “nonadaptive” characters. Results demonstrate that: (1) Phenotypic plasticity of wing pattern characters in response to temperature in laboratory-reared organisms is reminiscent of variation induced by seasonal change in the field. (2) Different wing pattern characters are under different control: “exposed” characters of butterflies at rest position are highly sensitive to temperature variation, whereas “hidden” characters, only visible during active behavior, are dominated by species differences. In general the sensitivity of the former can be attributed to their proposed function in deflecting predators. (3) The sexes differ especially in the size of those eyespots that are displayed during active behavior. (4) Species from seasonal and aseasonal environments react in a broadly similar manner to temperature variation. However, savannah species and species of aseasonal rainforest exhibit relatively shallow reaction norms, whereas reaction norms are steeper in species from the savannah-rainforest ecotone. Such a strong response was also apparent in so-called correlation networks between principal components for these species. (5) Phylogenetic distances are to some extent reflected in ordination in both PCA-space and DFA-space: closely related species of the safitza group remain close in both ordinations. The more distantly related species differ in ordination from a pattern as suggested by a phylogenetic reconstruction. It is argued that the wing pattern variation of these species reflects both adaptive processes and historical relationships.     

Relationship between chromosomal polymorphism and wing size in a natural population of Drosophila subobscura

Chromosomal polymorphism and wing size (as a measure of body size) were analysed simultaneously in two samples of Drosophila subobscura from Barcelona, Spain. The very rich chromosomal polymorphism of this species makes it difficult to detect the relationship of this polymorphism with any phenotypical character. However, a positive significant regression of wing size on the percentage of the autosome length with standard arrangement was found. Furthermore, for each polymorphic chromosome, except for the J chromosome, an association between the most frequent arrangements and wing size was observed. This trend, which was the same in the two samples, was that expected according to the latitudinal clines of both characters.     

Temperature dependence of development rate and adult size in Drosophila species: biophysical parameters

Adult size in Drosophila results from the ratio of the rate of biomass increase and the rate of differentiation, both rates being temperature sensitive. Data on rates and size are collected in two tropical and two temperate Drosophila species; differentiation rate is higher in the two tropical species, growth rate differs between the large and small species of similar climatic origin. A biophysical model is used to evaluate the temperature dependence of adult size in Drosophila. The model is based upon the Sharpe–Schoolfield equation connecting enzyme kinetics and biological rates. Temperature sensitivities of growth rate, development time, and wing and thorax size are characterized by biophysical parameters. The biophysical parameter indicating trait specific temperature sensitivity is lower in tropical species than in temperate species, both for growth rate and for differentiation rate. In the larger species of a climate pair, thorax size and wing size prove to differ in pattern of temperature dependence; in the smaller species of a geographical pair, thorax size and wing size have identical patterns of temperature dependence.     

Genetic variation and plasticity of thorax length and wing length in Drosophila aldrichi and D. buzzatii

Reaction norms across three temperatures of development were measured for thorax length, wing length and wing length/thorax length ratio for ten isofemale lines from each of two populations of Drosophila aldrichi and D. buzzatii. Means for thorax and wing length in both species were larger at 24 °C than at either 18 °C or 31 °C, with the reduction in size at 18 °C most likely due to a nutritional constraint. Although females were larger than males, the sexes were not different for wing length/thorax length ratio. The plasticity of the traits differed between species and between populations of each species, with genetic variation in plasticity similar for the two species from one locality, but much higher for D. aldrichi from the other. Estimates of heritabilities for D. aldrichi generally were higher at 18 °C and 24 °C than at 31 °C, but for D. buzzatii they were highest at 31 °C, although heritabilities were not significantly different between species at any temperature. Additive genetic variances for D. aldrichi showed trends similar to that for heritability, being highest at 18 °C and decreasing as temperature increased. For D. buzzatii, however, additive genetic variances were lowest at 24 °C. These results are suggestive that genetic variation for body size characters is increased in more stressful environments. Thorax and wing lengths showed significant genetic correlations that were not different between the species, but the genetic correlations between each of these traits and their ratio were significantly different. For D. aldrichi, genetic variation in the wing length/thorax length ratio was due primarily to variation in thorax length, while for D. buzzatii, it was due primarily to variation in wing length. The wing length/thorax length ratio, which is the inverse of wing loading, decreased linearly as temperature increased, and it is suggested that this ratio may be of greater adaptive significance than either of its components.     

Correlation between characters as related to developmental pattern in Drosophila

In order to better understand the genetic basis of some body traits and their correlations in Drosophila, in relation to their developmental history, a biometrical study was performed on three lines selected for short wing (fourth vein) and a control strain.The correlated response to selection for short wing and four body traits (thorax length and width, scutellar length, head width) and of eight other dimensional wing traits was considered.The results show a strong correlated response to selection of all wing traits, low correlations for the thorax characters, while head width remains relatively constant. Two groups of wing characters, corresponding to compartments of development, show different levels of covariation with the selected trait, the covariation being greater when the characters included in the same compartment of the selected trait are considered.The results are discussed in terms of developmental genetics of Drosophila and suggest that quantitative studies may be suitable for studying the rôle of interactions between sets of genes controlling development.     

Altitude and life‐history shape the evolution of Heliconius wings

Phenotypic divergence between closely related species has long interested biologists. Taxa that inhabit a range of environments and have diverse natural histories can help understand how selection drives phenotypic divergence. In butterflies, wing color patterns have been extensively studied but diversity in wing shape and size is less well understood. Here, we assess the relative importance of phylogenetic relatedness, natural history, and habitat on shaping wing morphology in a large dataset of over 3500 individuals, representing 13 Heliconius species from across the Neotropics. We find that both larval and adult behavioral ecology correlate with patterns of wing sexual dimorphism and adult size. Species with solitary larvae have larger adult males, in contrast to gregarious Heliconius species, and indeed most Lepidoptera, where females are larger. Species in the pupal‐mating clade are smaller than those in the adult‐mating clade. Interestingly, we find that high‐altitude species tend to have rounder wings and, in one of the two major Heliconius clades, are also bigger than their lowland relatives. Furthermore, within two widespread species, we find that high‐altitude populations also have rounder wings. Thus, we reveal novel adaptive wing morphological divergence among Heliconius species beyond that imposed by natural selection on aposematic wing coloration.     

Colonization of ephemeral detrital patches by vagile macroinvertebrates in a brackish lake: a body size-related process?

The mechanisms regulating the build-up of invertebrate assemblages on ephemeral detritus patches are still poorly understood. Here, the daily colonization of decaying reed leaves by vagile macroinvertebrates was monitored in an brackish lake in Italy. The highly variable abundance patterns of dominant taxa were analysed by spectral and geostatistical techniques to test for nonrandomness and to further determine whether they were related to body size. Comparisons between two contrasting sites allowed an assessment of the generality of our observations. At both sites, the macroinvertebrate assemblage was dominated by three detritivorous taxa, i.e. the isopod Lekanesphaera monodi, the amphipod Microdeutopus gryllotalpa and the polychaete Neanthes caudata. Overall, their abundance patterns were characterised by short-term fluctuations of a nonrandom, autocorrelated nature. In addition, a significant covariation was observed between the average body mass of each taxon and the complexity of the respective abundance pattern, expressed by the fractal dimension D. The covariation was observed at both study sites, notwithstanding the diverging outcomes of bivariate pattern comparisons for similar-sized taxa. Our findings indicate that the size of macroinvertebrates is strongly related to the short-term dynamics of their abundance patterns on reed detritus, suggesting that the interaction between vagile consumers and ephemeral resource patches might be influenced by individual energetics. The implications of size-related constraints for the coexistence of species on decaying detrital patches are discussed.     

Niche segregation among sympatric Amazonian teiid lizards

We examined standard niche axes (time, place, and food) for three sympatric teiid lizards in the Amazon rain forest. Activity times during the day were similar among species. Ameiva ameiva were in more open microhabitats and had higher body temperatures compared with the two species of Kentropyx. Microhabitat overlaps were low and not significantly different from simulations based on Monte Carlo analysis. Grasshoppers, crickets, and spiders were important in the diets of all three species and many relatively abundant prey were infrequently eaten (e.g., ants). Dietary overlaps were most similar between the two species of Kentropyx even though microhabitat overlaps were relatively low. A Monte Carlo analysis on prey types revealed that dietary overlaps were higher at all ranks than simulated overlaps indicating that use of prey is not random. Although prey size was correlated with lizard body size, there were no species differences in adjusted prey size. A. ameiva ate more prey items at a given body size than either species of Kentropyx. Body size varies among species, with A. ameiva being the largest and K. altamazonica the smallest. The two species of Kentropyx are most distant morphologically, with A. ameiva intermediate. The most distant species morphologically are the most similar in terms of prey types. A morphological analysis including 15 species from four genera revealed patterns of covariation that reflected phylogenetic affinities (i.e., taxonomic patterns are evident). A cluster analysis revealed that A. ameiva, K. pelviceps, and K. altamazonica were in the same morphological group and that within that group, A. ameiva differed from the rest of the species. In addition, K. pelviceps and K. altamazonica were distinguishable from other species of Kentropyx based on morphology. Received: 26 December 1998 / Accepted: 15 September 1999     

Patterns of genetic and morphometric differentiation in Melitaea (Mellicta) athalia (Lepidoptera: Nymphalidae)

Patterns of genetic and morphometric differentiation were surveyed in Melitaea (Mellicta) athalia populations of the Carpathian Basin. This species has a wide distribution and exists under a wide variety of ecological conditions. It has two ecotypes in Hungary: with either one or two broods per year. It is of particular interest to reveal the main factors driving differentiation patterns in this species. Samples in our study were obtained from five Hungarian and one Transylvanian (Romanian) regions. Enzyme polymorphism, wing characters and male external genitalia were analysed using traditional morphometric methods. Statistical methods were optimized to compare morphological and genetic data. The results of genetic surveys revealed a clear regional pattern of differentiation in M. athalia. Moreover, the results of principal component analysis, Bayesian clustering and the dendrogram all suggested that the regions can be classified into two groups corresponding to the East or West zones of the Carpathian Basin. In contrast, differentiation between the two ecotypes was less expressed in the genetic variation of M. athalia. Results of the analyses conducted on phenotypic variation also suggested a regional pattern for both sets of morphometric characters (wings and external genitalia). At the same time, neither East–West regional division nor ecotype differentiation was detected in the morphometric studies. In sum, our analyses confirmed that both genetic and phenotypic variations of M. athalia exhibit a regional pattern rather than the differentiation between the two ecotypes. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ?? , ??–??.     

Analysis of asymmetries in the African fruit bats Eidolon helvum and Rousettus egyptiacus (Mammalia: Megachiroptera) from the islands of the Gulf of Guinea. I. Variance and size components of bilateral variation

A set of cranial characters was examined in the fruit bats Rousettus egyptiacus and Eidolon helvum to compare trends and relative importance of major components of bilateral morphometric variation, and their relationship with character size. Using two‐way, sides‐by‐individuals ANOVA , four components of variation were estimated for each bilateral variable: individual variation (I), directional asymmetry (DA), non‐directional asymmetry (NDA) and measurement error (E). Both species exhibit similar major trends of variation in asymmetry across characters, as shown by principal component analysis, using variance components as variables. Degree of interspecific congruence among characters was confirmed by a two‐way ANOVA with species and variance components as fixed factors. Congruence of asymmetry patterns between species suggests that the concept of population asymmetry parameter (PAP) could be extended to higher hierarchies. PAPs above the species level may result from common mechanisms or similar developmental constraints acting on species’ buffering capacities and morphological integration processes.     

Hybridization and transgressive exploration of colour pattern and wing morphology in Heliconius butterflies

Hybridization can generate novel phenotypes distinct from those of parental lineages, a phenomenon known as transgressive trait variation. Transgressive phenotypes might negatively or positively affect hybrid fitness, and increase available variation. Closely related species of Heliconius butterflies regularly produce hybrids in nature, and hybridization is thought to play a role in the diversification of novel wing colour patterns despite strong stabilizing selection due to interspecific mimicry. Here, we studied wing phenotypes in first‐ and second‐generation hybrids produced by controlled crosses between either two co‐mimetic species of Heliconius or between two nonmimetic species. We quantified wing size, shape and colour pattern variation and asked whether hybrids displayed transgressive wing phenotypes. Discrete traits underlain by major‐effect loci, such as the presence or absence of colour patches, generate novel phenotypes. For quantitative traits, such as wing shape or subtle colour pattern characters, hybrids only exceed the parental range in specific dimensions of the morphological space. Overall, our study addresses some of the challenges in defining and measuring phenotypic transgression for multivariate traits and our data suggest that the extent to which transgressive trait variation in hybrids contributes to phenotypic diversity depends on the complexity and the genetic architecture of the traits.     

Correlated evolution of multivariate traits: detecting co-divergence across multiple dimensions

Tests of correlated evolution typically treat phenotypic characters as univariate variables, even though different trait attributes may contribute to their association with other traits. In this study, patterns of character covariation among species are analysed in a multivariate framework to test for both correlated rates and directions of evolutionary change in traits forming the genitalic complex of male grasshoppers. Although the covariation structure differs among traits, and among the constituent species of two grasshopper clades, significant co-divergence was detected among the most closely interacting genitalic traits (i.e. intromittent characters) in both clades. Co-divergence across shape space is not accompanied by similar rates of evolution among species, although the intromittent characters tend to show accelerated evolution (relative to nonintromittent characters). Differences in the evolutionary trajectories among traits may relate to their varied roles during mating. The study emphasizes the importance of a multivariate framework for detecting macroevolutionary patterns of correlated change.     

Geographic variation in Pemphigus populitransversus (Insecta: Aphididae)*†

The geographic variation of 33 morphological characters of two morphs of the gall-forming aphid Pemphigus populitransversus is studied in 214 locality samples. Among-locality variation ranges from 1 to 69% in the elongate morph and from 0 to 44% in the globular morph. The design of the study permits separation of interlocality correlations from intralocality correlations. The former are partly a function of the latter, confirming early observations on another Pemphigus species and on ticks. Factor analyses of both correlation matrices for both morphs yield four factors. Within localities these factors agree for the two morphs; among localities only one factor corresponds. Multiple discriminant analyses among localities of the two data sets do not correspond. There is little correlation between characters of stem mother and alate morphotypes within localities but such correlations are strong among localities. Maps are furnished for characters representing the independent dimensions of variation for each morph. Patterns of variation are shown to be significant by spatial autocorrelation analysis for both morphs but are much more marked in the elongate morph. Significant positive autocorrelation occurs up to 1000 km in the elongate morph – mostly only up to 200 km in the globular morph. There are two to three geographic variation patterns in the elongate morph, whereas in the globular morph the classes of patterns are less well defined and involve few characters. The environmental factors to which the globular and elongate morphs are adapting would appear to have different autocorrelation patterns. In each morph the patterns are clearly different and cannot be explained by a single microevolutionary process. The findings are compared with an earlier study in the related and largely sympatric P. populicaulis.     

Sex combs,allometry, and asymmetry in Drosophila

There has been recent debate about the expected allometry of sexually‐selected traits. Although sexually‐selected traits exhibit a diversity of allometric patterns, signalling characters are frequently positively allometric. By contrast, insect genitalia tend to be negatively allometric, although the allometry of nongenital sexually‐selected characters in insects is largely unknown (with some notable exceptions). It has also been suggested that there should be a negative association between the asymmetry and size of bilaterally‐paired, sexually‐selected traits, although this claim is controversial. We assessed the allometry and asymmetry (fluctuating asymmetry, FA) of a nongenital contact–courtship structure, the sex comb, in replicate populations of three species of Drosophila (we also measured wing FA). Sex combs are sexually‐selected characters used to grasp the female's abdomen and genitalia and to spread her wings prior to and during copulation. Although species differed in the size of the sex combs, all combs were positively allometric, and comb allometry did not generally differ significantly between species or populations. Comb and wing asymmetry did vary across species, although not across populations of the same species. However, FA was trait specific and was never negatively associated with trait size. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 923–934.     

De l'optimisation du nombre de variables morphologiques dans la discrimination entre populations (le cas de l'aile chez Drosophila melanogaster)

Whilst wing size measurements are often used in Drosophila to discriminate between groups of individuals, the choice of the particular characters measured is generally not justified.Statistical and genetical properties of 8 characters measured on the left wing, in three stocks of Drosophila melanogaster were analysed. A multivariate analysis is done by studying correlations between characters and by interpreting the first factor of a principal component analysis.The results shows that only one measurement is sufficient in order to discriminate between the stocks, as far as mean values are concerned; wing length is, in that case, the best character since its variance has a relatively high genetic component. When dealing with correlation among characters as a way of estimating shape, four measurements are needed and sufficient. This shows the necessity of choosing the characters to be measured.