Sexual dimorphism in traits related to locomotion: ontogenetic patterns of variation in Podarcis wall lizards

Sexual dimorphism in body size and shape in animals is normally linked to sexual selection mechanisms that modify the morphological properties of each sex. However, sexual dimorphism of ecologically relevant traits may be amplified by natural selection and result in the ecological segregation of both sexes. In the present study, we investigated patterns of sexual dimorphism of morphological traits relevant for locomotion in two lacertid lizards, Podarcis bocagei and Podarcis carbonelli, aiming to identify ontogenetic sources of variation. We analysed trunk and limb variation in relation to total body size, as well as the covariation of different traits, aiming to shed light on the proximate causation of adult sexual dimorphism. We find that, although immatures are generally monomorphic, adult females have a longer trunk, and adult males have longer fore and hind limbs. Both sexes differ substantially with respect to their growth trajectories and relationships between traits, whereas, in some cases, there are signs of morphological constraints delimiting the observed patterns. Because of the direct connection between limb size/shape and locomotor performance, which is relevant both for habitat use and escape from predators, the observed patterns of sexual dimorphism are expected to translate into ecological differences between both sexes. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 530–543.     

Digest: Evolution of camouflage patterns in geckos*

Is variation in geckos’ dorsal color patterns linked to specific camouflage strategies? In this article, Allen et al. investigate correlations at the interspecific level between color patterns and ecological traits, such as habitat or activity time, in 439 species of geckos.     

Squamate phylogeny, taxon sampling, and data congruence

To investigate the affinities of snakes, amphisbaenians and dibamids, the phylogenetic relationships among the major lineages (families) of extinct and extant squamates are assessed through a combined analysis of 248 osteological, 133 soft anatomical, and 18 ecological traits. The osteological data set represents a revision of previous data, taking into account recent criticism; the ecological data set is new. In addition, potentially critical fossil taxa (polyglyphanodontids and macrocephalosaurs) are included for the first time. The osteological and soft anatomical data sets each place snakes within anguimorphs, with dibamids and amphisbaenians near gekkotans. The putative primitive fossil amphisbaenian Sineoamphisbaena groups with macrocephalosaurs and polyglyphanodontids, together the sister group to scleroglossans. All three data sets are congruent, and these results are reinforced by combined analyses. In these, as in the osteological analyses, snakes are nested within marine lizards. However, exclusion of fossil taxa from the osteological data set results in a ‘limbless clade’ consisting of snakes, amphisbaenians and dibamids, and introduces significant conflict between osteology and soft anatomy. Also, deletion tests and character weighting reveal that the signal in the reduced osteological data set is internally contradictory. These results increase confidence in the arrangement supported by the all-taxon osteological, the soft anatomical, and the combined data, and suggest that exclusion of fossils confounds the signal in the osteological data set. Finally, the morphological data support the nesting of snakes within marine lizards, and thus a marine origin of snakes. This result still holds when relationships between living forms are constrained to the topology suggested by molecular sequences: if marine lizards are allowed to ‘float’ within this molecular framework, they form the stem group to snakes, and do not group with varanids as previously suggested.See also Electronic Supplement at: http://www.senckenberg.de/odes/05-04.htm.     

Ecomorphological patterns of aerial feeding in oscines (Passeriformes: Passeri)

The hindlimb (myology and osteology) of swallows (Hirundinidae) is studied and compared with that of seven other passerine families to identify ecomorphological patterns. Muscular and osteological differences are found among swallow species and associations between morphology and foraging technique are examined. We explain morphological differences found in hirundinids as adaptations favouring flexion and adduction of the legs in these aerial foragers, which devote very little time to cursorial locomotion. This adaptive hypothesis is tested using a phylogenetic approach on the basis of an available molecular phylogenetic hypothesis. A clear ecomorphological pattern emerges relating foraging behaviour and pelvic morphology in hirundinids: aerial feeding technique is correlated with short distal leg segments, a large pelvis, a medial insertion of M. iliotibialis cranialis, an absence of pars accessoria of M. flexor cruris lateralis and a fused M. pubo-ischiofemoralis.     

THE EVOLUTION OF THE SEXUALLY SELECTED SWORD IN XIPHOPHORUS DOES NOT COMPROMISE AEROBIC LOCOMOTOR PERFORMANCE

Sexual selection can increase morphological diversity within and among species. Little is known regarding how interspecific variation produced through sexual selection affects other functional systems. Here, we examine how morphological diversity resulting from sexual selection impacts aerobic locomotor performance. Using Xiphophorus (swordtail fish) and their close relatives (N = 19 species), we examined whether the evolution of a longer sexually selected sword affects critical swimming speed. We also examined the effect of other suborganismal, physiological, and morphological traits on critical swimming speed, as well as their relationship with sword length. In correlation analyses, we found no significant relationship between sword length and critical swimming speed. Unexpectedly, we found that critical swimming speed was higher in species with longer swords, after controlling for body size in multiple regression analyses. We also found several suborganismal and morphological predictors of critical swimming speed, as well as a significant negative relationship between sword length and heart and gill mass. Our results suggest that interspecific variation in sword length is not costly for this aspect of swimming performance, but further studies should examine potential costs for other types of locomotion and other components of Darwinian fitness (e.g., survivorship, life span).     

Effects of assortative mate choice on the genomic and morphological structure of a hybrid zone between two bird subspecies

Phenotypic differentiation plays an important role in the formation and maintenance of reproductive barriers. In some cases, variation in a few key aspects of phenotype can promote and maintain divergence; hence, the identification of these traits and their associations with patterns of genomic divergence is crucial for understanding the patterns and processes of population differentiation. We studied hybridization between the alba and personata subspecies of the white wagtail (Motacilla alba), and quantified divergence and introgression of multiple morphological traits and 19,437 SNP loci on a 3,000 km transect. Our goal was to identify traits that may contribute to reproductive barriers and to assess how variation in these traits corresponds to patterns of genome‐wide divergence. Variation in only one trait—head plumage patterning—was consistent with reproductive isolation. Transitions in head plumage were steep and occurred over otherwise morphologically and genetically homogeneous populations, whereas cline centres for other traits and genomic ancestry were displaced over 100 km from the head cline. Field observational data show that social pairs mated assortatively by head plumage, suggesting that these phenotypes are maintained by divergent mating preferences. In contrast, variation in all other traits and genetic markers could be explained by neutral diffusion, although weak ecological selection cannot be ruled out. Our results emphasize that assortative mating may maintain phenotypic differences independent of other processes shaping genome‐wide variation, consistent with other recent findings that raise questions about the relative importance of mate choice, ecological selection and selectively neutral processes for divergent evolution.     

Morphology of the Podarcis wall lizards (Squamata: Lacertidae) from the Iberian Peninsula and North Africa: patterns of variation in a putative cryptic species complex

Cryptic species complexes represent groups that have been classified as a single species, because of the difficulty in distinguishing its members morphologically. Morphological investigation following the discovery of cryptic diversity is crucial for describing and conserving biodiversity. Here we present a detailed account of morphological variation in a group of Iberian and North African Podarcis wall lizards of the family Lacertidae, trying to elucidate the morphological patterns observed between known mitochondrial lineages. Our results reveal very high morphological variation within lineages, considering both biometric and pholidotic traits, but also indicate that lineages are significantly different from each other. The main sources of variation, both globally and between lineages, arise from body size, head dimensions, and limb length, possibly pointing to underlying ecological mechanisms. A combination of body size, body shape, and continuous pholidotic traits allows a relatively good discrimination between groups, especially when comparing one group with the rest or pairs of groups. However, ranges of variation greatly overlap between groups, thereby not allowing the establishment of diagnostic traits. The high morphological variation observed indicates that external morphology is not particularly useful for species delimitation in this group of lizards, as local adaptation seems to play a major role in within‐ and between‐group differentiation. © 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2012, 164 , 173–193.     

Assessing concurrent patterns of environmental niche and morphological evolution among species of horned lizards (Phrynosoma)

The prediction that variation in species morphology is related to environmental features has long been of interest to ecologists and evolutionary biologists. Many studies have demonstrated strong associations between morphological traits and local habitat characteristics, but few have considered the extent to which morphological traits may be associated with environmental features across broad geographic areas. Here, we use morphological, environmental and phylogenetic data compiled from Phrynosoma species to examine morphological and climatic variation across the geographic ranges of these species in an evolutionary context. We find significant phylogenetic signal in species’ environmental niches, but not in morphological traits. Furthermore, we demonstrate a significant correlation between species’ environmental niches and morphological traits when phylogenetic history is accounted for in the analysis. Our results suggest the importance of climatic variables in influencing morphological variation among species, and have implications for understanding how species distributions are constrained by environmental variation.     

Sexual differences in locomotor performance in Tropidurus catalanensis lizards (Squamata: Tropiduridae) – body shape,size and limb musculature explain variation between males and females

Sexual dimorphism (SD) is the evolutionary outcome of selection acting differently on males and females. Several studies describe sexual differences in body size, although other morphological traits might be allometric between sexes and imply functional consequences. Here we test whether morphological differences between sexes in size and shape in the lizard Tropidurus catalanensis explain variation in performance of four locomotor traits. Our results show that males are larger than females and also exhibit longer limbs, longer muscles and larger muscle cross‐sectional areas, while females have longer trunks and more sharped anterior claws; males outperform females in all locomotor performances measured. Sexual differences in sprinting and climbing is related with body size, and climbing performance is also explained by limb lengths, by differences in lengths and cross‐sectional areas of specific muscles, and by interlimb distances. Between‐sex differences in exertion are also related to SD, despite associations with sharper posterior claws that are independent of sex. Grasping performance, however, is associated with some muscle and morphological parameters that are not sexually dimorphic. Together our results suggest that morphology might be under sexual selection in T. catalanensis, given that better locomotor performance likely favours male lizards in typical activities of this polygenic species, such as territory defence and female acquisition. Moreover, the longer trunks that characterize females may confer more space to accommodate eggs. On the other hand, territory defence by males probably increases their exposure to predators, resulting in a synergistic effect of sexual and natural selection in the evolution of SD in T. catalanensis.     

A Comparison of Qualitative and Quantitative Methodological Approaches to Characterizing the Dorsal Side of the Scapula in Hominoidea and Its Relationship to Locomotion

Hominoidea have adapted to various forms of locomotion, each of which has specific requirements that are reflected in the shape of the scapula. We compared several qualitative and quantitative methods for characterizing the dorsal side of the scapula to detect morphological differences that reflect the adaptations of the scapula to locomotor behaviors. Our sample included 55 specimens of Hominoidea, representing five genera, including Homo, focusing specifically on the relative sizes of the scapular supraspinous and infranspinous fossae. In addition, we weighed the supraspinatus and infraspinatus muscles of 23 of the specimens to examine the feasibility of extrapolating muscle characteristics from osteological data. Our findings confirmed that the five genera exhibit significant differences in the relative size of the supraspinous and the infraspinous fossae that are related to their forms of locomotion. The supraspinous fossa was relatively small in Homo and Pongo but large in Pan, Gorilla, and Hylobates. The analysis of muscle weights showed that a substantial amount of information about soft tissues is lost in osteological analyses, leading us to recommend caution when drawing conclusions regarding forms of locomotion based only on osteological analyses.     

From the inside out: Discovery of a new genus of threadsnakes based on anatomical and molecular data,with discussion of the leptotyphlopid hemipenial morphology

The systematics of Leptotyphlopidae is historically controversial mostly due to their conserved external morphology in comparison with other snakes. However, recent studies have stressed that anatomical data might be informative for clarifying the leptotyphlopid taxonomy and evolution. We erect a new genus to accommodate Leptotyphlops collaris based on evidence from osteology, hemipenial morphology, and molecular data. We also provide expanded data regarding the intraspecific variation based on additional specimens collected in field trips and literature data, performing detailed comparisons among the new genus and all other New World leptotyphlopids. The new genus is distinguished from other leptotyphlopids by its unique hemipenial morphology and its exclusive combination of osteological and external morphology characters, with molecular data also supporting the new generic arrangement. We also provide a comprehensive discussion of the hemipenial morphology for the subfamily Epictinae based on literature and novel data gathered herein.     

Repeated evolution of digital adhesion in geckos: a reply to Harrington and Reeder

We published a phylogenetic comparative analysis that found geckos had gained and lost adhesive toepads multiple times over their long evolutionary history (Gamble et al., PLoS One, 7, 2012, e39429). This was consistent with decades of morphological studies showing geckos had evolved adhesive toepads on multiple occasions and that the morphology of geckos with ancestrally padless digits can be distinguished from secondarily padless forms. Recently, Harrington & Reeder (J. Evol. Biol., 30, 2017, 313) reanalysed data from Gamble et al. (PLoS One, 7, 2012, e39429) and found little support for the multiple origins hypothesis. Here, we argue that Harrington and Reeder failed to take morphological evidence into account when devising ancestral state reconstruction models and that these biologically unrealistic models led to erroneous conclusions about the evolution of adhesive toepads in geckos.     

Historical and ecological influence in the evolutionary diversification of external morphology of neotropical spiny rats (Echimyidae,Rodentia)

The radiation of neotropical echimyid rodents resulted in the diversification of spiny rats, hutias, and the coypu, grouped into four major clades. Different echimyid lineages specialized for terrestrial, semifossorial, semiaquatic, and arboreal locomotion, and for living in bamboo thickets. Comparative phylogenetic methods were herein used for evaluating the relative effect of historical and ecological factors in shaping morphometric traits of external morphology (length of head and body, tail, ear, and hindfeet). Additionally, we investigated whether the adoption of different locomotory habits was associated with changes in their macroevolutionary dynamics. Our findings showed that variation of all traits was phylogenetically structured, although size was less structured than other traits. Tail, ear, and mainly hindfeet were allometrically correlated with head and body length, indicating the occurrence of evolutionary structural constraints. In addition to phylogenetic and allometric components, morphometric variation was strongly associated with locomotory specializations, except for body size. Disparification of body size and tail length took place gradually, fitting the Brownian motion model albeit with some punctual shifts in evolutionary rates. Some of these shifts were associated with changes in locomotory habits, notably with adoption of a semiaquatic habit by the large‐sized Myocastor lineage, which occurred with an accelerated rate of size evolution. Evolutionary changes in ear and hindfeet length were concentrated during early echimyid diversification, concomitantly with the emergence of most locomotory habits, with subsequent deceleration of evolutionary rates. These findings indicated a complex interaction between phylogenetic, structural, and ecological effects gradually shaping echimyid external morphology.     

Associations between physical isolation and geographical variation within three species of Neotropical birds

We studied effects of physical isolation on geographical variation in mtDNA RFLP polymorphisms and a suite of morphological characters within three species of neotropical forest birds; the crimson-backed tanager Ramphocelus dimidiatus, the blue-gray tanager Thraupis episcopus, and the streaked saltator Saltator albicollis. Variation among populations within continuous habitat on the Isthmus of Panama was compared with that among island populations isolated for about 10000 years. Putative barriers to dispersal were influential, but apparent isolation effects varied by species, geographical scale, and whether molecular or morphological traits were being assessed. We found no geographical structuring among the contiguous, mainland sampling sites. Migration rates among the islands appeared sufficient to maintain homogeneity in mtDNA haplotype frequencies. In contrast, variation in external morphology among islands was significant within two of three species. For all species, we found significant variation in genetic and morphological traits between the island (collectively) and mainland populations. Interspecific variation in the effects of isolation was likely related to differential vagility. These data generally corroborate other studies reporting relatively great geographical structuring within tropical birds over short distances. Behaviourally based traits - low vagility and high ‘sensitivity’ to geographical barriers - may underlie extensive diversification within neotropical forest birds, but more extensive ecological and phylogeographic information are needed on a diverse sample of species.     

Constraints on the evolution of phenotypic plasticity in the clonal plant Hydrocotyle vulgaris

The evolution of phenotypic plasticity of plant traits may be constrained by costs and limits. However, the precise constraints are still unclear for many traits under different ecological contexts. In a glasshouse experiment, we grew ramets of 12 genotypes of a clonal plant Hydrocotyle vulgaris under the control (full light and no flood), shade and flood conditions and tested the potential costs and limits of plasticity in 13 morphological and physiological traits in response to light availability and flood variation. In particular, we used multiple regression and correlation analyses to evaluate potential plasticity costs, developmental instability costs and developmental range limits of each trait. We detected significant costs of plasticity in specific petiole length and specific leaf area in response to shade under the full light condition and developmental range limits in specific internode length and intercellular CO₂ concentration in response to light availability variation. However, we did not observe significant costs or limits of plasticity in any of the 13 traits in response to flood variation. Our results suggest that the evolution of phenotypic plasticity in plant traits can be constrained by costs and limits, but such constraints may be infrequent and differ under different environmental contexts.     

小叶锦鸡儿天然居群叶形态性状变异研究

为揭示小叶锦鸡儿(Caragana microphylla)天然居群叶形态性状的变异规律及其生态适应性特征,该研究以10个小叶锦鸡儿天然居群为对象,通过多重比较、巢式方差分析、相关性分析、聚类分析和主成分分析等方法,对7个叶形态性状进行分析。结果表明：(1)小叶锦鸡儿叶形态性状在居群内和居群间均存在极显著差异(P < 0.01),平均变异系数为10.13%,不同性状的变异幅度为6.23%~12.78%;平均叶形态性状的表型分化系数为43.62%,居群内变异(30.09%)大于居群间变异(24.91%),说明居群内是其叶形态性状变异的主要来源。(2)相关性分析表明,环境因子对小叶锦鸡儿的叶形态性状变异有很大的影响,在地理空间上主要呈现出沿海拔梯度的变异模式;主成分分析的结果显示,小叶宽、叶柄宽和叶柄长对小叶锦鸡儿叶形态变异起主导作用;利用欧式距离对小叶锦鸡儿居群进行UPGMA聚类分析结果显示,基于叶形态性状和环境因子可分别将小叶锦鸡儿10个居群分为3类和2类,Mantel检验结果表明,小叶锦鸡儿的叶形态性状变异不存在地理连续性。研究结果为小叶锦鸡儿的适应性进化和开发利用提供了理论依据。     

Variation in Body Shape across Species and Populations in a Radiation of Diaptomid Copepods

Inter and intra-population variation in morphological traits, such as body size and shape, provides important insights into the ecological importance of individual natural populations. The radiation of Diaptomid species (~400 species) has apparently produced little morphological differentiation other than those in secondary sexual characteristics, suggesting sexual, rather than ecological, selection has driven speciation. This evolutionary history suggests that species, and conspecific populations, would be ecologically redundant but recent work found contrasting ecosystem effects among both species and populations. This study provides the first quantification of shape variation among species, populations, and/or sexes (beyond taxonomic illustrations and body size measurements) to gain insight into the ecological differentiation of Diaptomids. Here we quantify the shape of five Diaptomid species (family Diaptomidae) from four populations each, using morphometric landmarks on the prosome, urosome, and antennae. We partition morphological variation among species, populations, and sexes, and test for phenotype-by-environment correlations to reveal possible functional consequences of shape variation. We found that intraspecific variation was 18-35% as large as interspecific variation across all measured traits. Interspecific variation in body size and relative antennae length, the two traits showing significant sexual dimorphism, were correlated with lake size and geographic location suggesting some niche differentiation between species. Observed relationships between intraspecific morphological variation and the environment suggest that divergent selection in contrasting lakes might contribute to shape differences among local populations, but confirming this requires further analyses. Our results show that although Diaptomid species differ in their reproductive traits, they also differ in other morphological traits that might indicate ecological differences among species and populations.