Interspecific Morphological Variation Research Articles

Sexual dimorphism, allometry, and interspecific variation in the cranial morphology of seven Meriones species (Gerbillinae, Rodentia)

Sexual dimorphism, allometry, and interspecific variation in the cranial morphology of seven Meriones species (Gerbillinae, Rodentia)

Comparative Plastid Genomes of Primula Species: Sequence Divergence and Phylogenetic Relationships

Compared to traditional DNA markers, genome-scale datasets can provide mass information to effectively address historically difficult phylogenies. Primula is the largest genus in the family Primulaceae, with members distributed mainly throughout temperate and arctic areas of the Northern Hemisphere. The phylogenetic relationships among Primula taxa still maintain unresolved, mainly due to intra- and interspecific morphological variation, which was caused by frequent hybridization and introgression. In this study, we sequenced and assembled four complete plastid genomes (Primula handeliana, Primula woodwardii, Primula knuthiana, and Androsace laxa) by Illumina paired-end sequencing. A total of 10 Primula species (including 7 published plastid genomes) were analyzed to investigate the plastid genome sequence divergence and their inferences for the phylogeny of Primula. The 10 Primula plastid genomes were similar in terms of their gene content and order, GC content, and codon usage, but slightly different in the number of the repeat. Moderate sequence divergence was observed among Primula plastid genomes. Phylogenetic analysis strongly supported that Primula was monophyletic and more closely related to Androsace in the Primulaceae family. The phylogenetic relationships among the 10 Primula species showed that the placement of P. knuthiana–P. veris clade was uncertain in the phylogenetic tree. This study indicated that plastid genome data were highly effective to investigate the phylogeny.

AutoMorph: Accelerating morphometrics with automated 2D and 3D image processing and shape extraction

Abstract Large‐scale, comparative studies of morphological variation are rare due to the time‐intensive nature of shape quantification. This data gap is important to address, as intraspecific and interspecific morphological variation underpins and reflects ecological and evolutionary processes. Here, we detail a novel software package, AutoMorph, for high‐throughput object and shape extraction. AutoMorph can batch image many types of organisms (e.g. foraminifera, molluscs and fish teeth), allowing for rapid generation of assemblage‐scale morphological data. We used AutoMorph to image and generate 2D and 3D morphological data for >100,000 marine microfossils in about a year. Our collaborators have used AutoMorph to process >12,000 patellogastropod shells and >50,000 fish teeth. AutoMorph allows users to rapidly produce large amounts of morphological data, facilitating community‐scale evolutionary and ecological studies. To hasten the adoption of automated approaches, we have made AutoMorph freely available and open source. AutoMorph runs on all UNIX‐like systems; future versions will run across all platforms.

New species and phylogeny of landhoppers in the genus Waematau Duncan, 1994 (Crustacea: Amphipoda: Talitridae) from northern New Zealand

The talitrid landhopper genus Waematau Duncan, 1994 is restricted to the northern North Island of New Zealand. Six species of Waematau from Te Paki Ecological District are documented. Three known species, Waematau muriwhenua Duncan, 1994, W. reinga Duncan, 1994 and W. unuwhao Duncan, 1994, are redescribed and three new species, W. kohuroa sp. nov., W. rereke sp. nov. and W. ringanohinohi sp. nov. are described, bringing the total number of known Waematau species to eight. A molecular phylogenetic analysis of all eight known Waematau species was conducted using DNA sequences from the CO1, 16S and histone H3 loci. Results show a high degree of congruence between the molecular phylogeny and morphological characters distinguishing the species. Molecular analysis also supports recognition of the three new species, despite low levels of interspecific morphological variation for certain traits. We identify the most obvious morphological indicators of evolutionary change between closely related species of Waematau, and predict that the New Zealand landhopper fauna is richer than currently recognised.

Beyond the carapace: skull shape variation and morphological systematics of long-nosed armadillos (genus Dasypus).

BackgroundThe systematics of long-nosed armadillos (genus Dasypus) has been mainly based on a handful of external morphological characters and classical measurements. Here, we studied the pattern of morphological variation in the skull of long-nosed armadillos species, with a focus on the systematics of the widely distributed nine-banded armadillo (Dasypus novemcinctus).MethodsWe present the first exhaustive 3D comparison of the skull morphology within the genus Dasypus, based on micro-computed tomography. We used geometric morphometric approaches to explore the patterns of the intra- and interspecific morphological variation of the skull with regard to several factors such as taxonomy, geography, allometry, and sexual dimorphism.ResultsWe show that the shape and size of the skull vary greatly among Dasypus species, with Dasypus pilosus representing a clear outlier compared to other long-nosed armadillos. The study of the cranial intraspecific variation in Dasypus novemcinctus evidences clear links to the geographic distribution and argues in favor of a revision of past taxonomic delimitations. Our detailed morphometric comparisons detected previously overlooked morphotypes of nine-banded armadillos, especially a very distinctive unit restricted to the Guiana Shield.DiscussionAs our results are congruent with recent molecular data and analyses of the structure of paranasal sinuses, we propose that Dasypus novemcinctus should be regarded either as a polytypic species (with three to four subspecies) or as a complex of several distinct species.

A unifying explanation for variation in ozone sensitivity among woody plants.

Tropospheric ozone is considered the most detrimental air pollutant for vegetation at the global scale, with negative consequences for both provisioning and climate regulating ecosystem services. In spite of recent developments in ozone exposure metrics, from a concentration-based to a more physiologically relevant stomatal flux-based index, large-scale ozone risk assessment is still complicated by a large and unexplained variation in ozone sensitivity among tree species. Here, we explored whether the variation in ozone sensitivity among woody species can be linked to interspecific variation in leaf morphology. We found that ozone tolerance at the leaf level was closely linked to leaf dry mass per unit leaf area (LMA) and that whole-tree biomass reductions were more strongly related to stomatal flux per unit leaf mass (r2 =0.56) than to stomatal flux per unit leaf area (r2 =0.42). Furthermore, the interspecific variation in slopes of ozone flux-response relationships was considerably lower when expressed on a leaf mass basis (coefficient of variation, CV=36%) than when expressed on a leaf area basis (CV=66%), and relationships for broadleaf and needle-leaf species converged when using the mass-based index. These results show that much of the variation in ozone sensitivity among woody plants can be explained by interspecific variation in LMA and that large-scale ozone impact assessment could be greatly improved by considering this well-known and easily measured leaf trait.

Towards a functional understanding of species coexistence: ecomorphological variation in relation to whole‐organism performance in two sympatric lizards

SummaryWe examined intra‐ and interspecific variation in functional morphology and whole‐organism performance in a sympatric lizard species pair,Iberolacerta horvathiandPodarcis muralis, in the area with a high potential for competition.The biggest variation between species was found in two functional traits, bite force and climbing speed, linked with corresponding morphological traits.The species with larger and taller heads,P. muralis, exhibited correspondingly stronger bite forces. The other species exhibited smaller and flatter head. Both traits may potentially promote segregation between species in trophic niche (stronger bites relate to harder prey) and in refuge use (flatter heads allow using narrower crevices, hence, influencing escaping from common predators). Stronger bites and larger heads also provide one species with a dominant position in interspecific agonistic interactions.Females had longer trunks that impacted negatively on climbing speed, which may lower anti‐predator escape abilities of the more trunk‐dimorphic species, but positively influence reproductive effort.Our results exemplify how the joint examination of morphological and functional traits of ecologically similar and sympatric species can provide a mechanistic background for understanding their coexistence, namely, syntopic populations that are frequent in the study area.The identified roles of functional morphology in this system of sympatric rock lizards support the contribution of functional diversification for the complexity of community structure via coexistence.Alay summaryis available for this article.

Digital Morphometrics of Two North American Grapevines (Vitis: Vitaceae) Quantifies Leaf Variation between Species, within Species, and among Individuals.

Recent studies have demonstrated that grapevine (Vitis spp.) leaf shape can be quantified using digital approaches which indicate phylogenetic signal in leaf shape, discernible patterns of developmental context within single leaves, and signatures of local environmental conditions. Here, we extend this work by quantifying intra-individual, intraspecific, and interspecific variation in leaf morphology in accessions of North American Vitis riparia and V. rupestris in a common environment. For each species at least four clonal replicates of multiple genotypes were grown in the Missouri Botanical Garden Kemper Center for Home Gardening. All leaves from a single shoot were harvested and scanned leaf images were used to conduct generalized Procrustes analysis, linear discriminant analysis, and elliptical Fourier analysis. Leaf shapes displayed genotype-specific signatures and species distinctions consistent with taxonomic classifications. Leaf shape variation within genotypes and among clones was the result of pest and pathogen-induced leaf damage that alters leaf morphology. Significant trends in leaf damage caused by disease and infestation were non-random with respect to leaf position on the shoot. Digital morphometrics is a powerful tool for assessing leaf shape variation among species, genotypes, and clones under common conditions and suggests biotic factors such as pests and pathogens as important drivers influencing leaf shape.

Ecological niche partitioning within a large predator guild in a nutrient‐limited estuary

AbstractWithin oligotrophic ecosystems, resource limitations coupled with interspecific variation in morphology, physiology, and life history traits may lead to niche partitioning among species. How generalist predators partition resources and their mechanisms, however, remain unclear across many ecosystems. We quantified niche partitioning among upper trophic level coastal and estuarine species: American alligators (Alligator mississippiensis), bull sharks (Carcharhinus leucas), common bottlenose dolphins (Tursiops truncatus), common snook (Centropomus undecimalis), and Atlantic tarpon (Megalops atlanticus) in the Shark River Estuary of the Florida Coastal Everglades, USA using acoustic telemetry, stable isotope analysis, and visual surveys, combined with published diet and life history demographic information. Spatial and isotopic niche overlap occurred among most species, with variability in partitioning among interspecific interactions. However, seasonal variability in habitat use, movements patterns, and trophic interactions may promote coexistence within this resource‐limited estuary. Beyond guild‐level niche partitioning, predators within the Shark River Estuary also exhibit partitioning within species through individual specializations and divergent phenotypes, which may lead to intraspecific variability in niche overlap with other predators. Niche differentiation expressed across multiple organizational levels (i.e., populations and communities) coupled with behavioral plasticity among predators in oligotrophic ecosystems may promote high species diversity despite resource limitations, which may be important when species respond to natural and human‐driven environmental change.

Nutrient foraging strategies are associated with productivity and population growth in forest shrubs.

Temperate deciduous forest understoreys are experiencing widespread changes in community composition, concurrent with increases in rates of nitrogen supply. These shifts in plant abundance may be driven by interspecific differences in nutrient foraging (i.e. conservative vs. acquisitive strategies) and, thus, adaptation to contemporary nutrient loading conditions. This study sought to determine if interspecific differences in nutrient foraging could help explain patterns of shrub success and decline in eastern North American forests. Using plants grown in a common garden, fine root traits associated with nutrient foraging were measured for six shrub species. Traits included the mean and skewness of the root diameter distribution, specific root length (SRL), C:N ratio, root tissue density, arbuscular mycorrhizal colonization and foraging precision. Above- and below-ground productivity were also determined for the same plants, and population growth rates were estimated using data from a long-term study of community dynamics. Root traits were compared among species and associations among root traits, measures of productivity and rates of population growth were evaluated. Species fell into groups having thick or thin root forms, which correspond to conservative vs. acquisitive nutrient foraging strategies. Interspecific variation in root morphology and tissue construction correlated with measures of productivity and rates of cover expansion. Of the four species with acquisitive traits, three were introduced species that have become invasive in recent decades, and the fourth was a weedy native. In contrast, the two species with conservative traits were historically dominant shrubs that have declined in abundance in eastern North American forests. In forest understoreys of eastern North America, elevated nutrient availability may impose a filter on species success in addition to above-ground processes such as herbivory and overstorey canopy conditions. Shrubs that have root traits associated with rapid uptake of soil nutrients may be more likely to increase in abundance, while species without such traits may be less likely to keep pace with more productive species.

Sexual dimorphism in the carapace shape and length of the freshwater palaemonid shrimp Macrobrachium potiuna (Müller, 1880) (Decapoda: Caridea: Palaemonidae): geometric and traditional morphometric approaches

Sexual dimorphism is characterized by morphological, physiological, or behavioral differences between males and females. The genus Macrobrachium is a diverse group of freshwater shrimps distributed throughout tropical and subtropical regions. They have a great intra- and interspecific morphological variation, with some species showing sexual dimorphism. We investigated the sexual dimorphism of the size and shape of the carapace and body weight of Macrobrachium potiuna (Müller, 1880) in three populations of the State of Paraná through traditional and geometric morphometric techniques. The populations were sampled from three rivers: the Pombas River, Coastal Basin, the Piraquara River, First Plateau, and the Guabiroba River, Second Plateau. Morphometric analyses indicated that male shrimps showed differences in carapace length and body weight: the higher the distance from the sea, the smaller and lighter the shrimps. Carapace shape also differed significantly between the sexes in all three populations, with males having a less robust carapace, but a more elongated rostrum than females. The morphological differences between the genders seem to reflect the reproductive roles of males and females in this environment.

In vivo bone strain in the mandibular corpus of Sapajus during a range of oral food processing behaviors

It has been hypothesized that mandibular corpus morphology of primates is related to the material properties of the foods that they chew. However, chewing foods with different material properties is accompanied by low levels of variation in mandibular strain patterns in macaques. We hypothesized that if variation in primate mandible form reflects adaptations to feeding on foods with different material and geometric properties, then this variation will be driven primarily by differences in oral food processing behavior rather than differences in chewing per se. To test this hypothesis, we recorded in vivo bone strain data from the lateral and medial surfaces of the mandibular corpus during complete feeding sequences in three adult male Sapajus as they fed on foods with a range of sizes and material properties. We assessed whether variation in mandibular corpus strain regimes is associated with variation in feeding behaviors and/or chewing on different foods, and we quantified the relative variation in mandibular corpus strain regimes associated with chewing on foods of different material properties versus a range of oral food processing behaviors (incisor, premolar, and molar biting; pulling on incisors; mastication). Feeding behavior had a significant effect on mandibular corpus strain regimes, as did chewing side and the cycle number in a feeding sequence. However, food type had weaker effects and usually only through interaction effects with chewing side and/or cycle type. Strain regimes varied most across different chew sides, then across different behaviors, and lastly between mastication cycles on different foods. Strain magnitudes associated with premolar, molar, and incisor biting were larger than those recorded during mastication. These data suggest that intra- and inter-specific variation in mandible morphology is a trade-off between performance requirements of different oral food processing behaviors and of variation in chewing side, with direct effects of food type being less important.

On the growth of the largest living rodent: Postnatal skull and dental shape changes in capybara species (Hydrochoerus spp.)

We report on intraspecific and interspecific morphological variation in the cranium, mandible and teeth along the ontogenetic trajectories of the two species of the largest living rodent, the capybara. A three dimensional geometric morphometrics approach was used to compare 171 Hydrochoerus hydrochaeris and 44 Hydrochoerus isthmius specimens ranging from newborn to adult. The specimens were assigned to seven different age classes according to cranial suture closure. The species can be differentiated in the morphospace occupation. They differ in the angle between the braincase and rostrum—H. hydrochaeris displays a straight transition whereas the snout of H. isthmius is inclined ventrally. The males in both species are bigger than the females, but no shape differences were detected. The youngest two age classes (up to 0.5 months and 0.5–10 months; before reaching sexual maturity) can be morphologically differentiated from the older age classes. Shape changes during growth are similar in both species: with increasing age, the round neurocranium flattens and the proportionally short snout elongates. Moreover, both species follow similar ontogenetic trajectories. H. hydrochaeris and H. isthmius can be differentiated by size and shape; the shape differences may indicate differences in diet and habitat. This study illustrates the relevance of an ontogenetic perspective to characterize species and examine the bases of disparity in adults. Furthermore, variation recorded in dental features serves to evaluate taxonomic and evolutionary aspects in fossil capybaras.

Scale Characteristics of Four Goatfishes (Family Mullidae) from Mediterranean Sea at Alexandria, Egypt

Scale Characteristics of Four Goatfishes (Family Mullidae) from Mediterranean Sea at Alexandria, Egypt The scale characteristics study has aimed to deal with the taxonomic and biological aspects of four mullid species (Family Mullidae), Mullus sermuletus, Mullus barbatus, Upeneus moluccensis and Upeneus pori from the Mediterranean Sea at Alexandria, Egypt. The characteristics of scales of the four mullid species considered were studied in the term of morphometry and scanning electron microscopic techniques. A great variety of size free intra- and interspecific scale surface morphological variations was revealed. The present work on scale characteristics of the four mullid species studied the overall form of the scales and their morphometrics, radii number, shape of interradial tongues and first circuli, form of interradial circuli and their denticles, the outer rostolateral and inner rostolateral circuli and the form of their denticles, granulation of the caudal field and the shape of ctenii. Among the scale characteristics used to discriminate between the four mullid species studied are the unique form and branching patterns of the lateral line canal. These findings were discussed in terms of their functional morphology in comparison with respect to other teleost fishes.

Ecogeographical Variation in Skull Shape of South-American Canids: Abiotic or Biotic Processes?

Species morphological changes can be mutually influenced by environmental or biotic factors, such as competition. South American canids represent a quite recent radiation of taxa that evolved forms very disparate in phenotype, ecology and behaviour. Today, in the central part of South America there is one dominant large species (the maned wolf, Chrysocyon brachyurus) that directly influence sympatric smaller taxa via interspecific killing. Further south, three species of similar sized foxes (Lycalopex spp.) share the same habitats. Such unique combination of taxa and geographic distribution makes South American dogs an ideal group to test for the simultaneous impact of climate and competition on phenotypic variation. Using geometric morphometrics, we quantified skull size and shape of 431 specimens belonging to the eight extant South American canid species: Atelocynus microtis, Cerdocyon thous, Ch. brachyurus, Lycalopex culpaeus, L. griseus, L. gymnocercus, L. vetulus and Speothos venaticus. South American canids are significantly different in both skull size and shape. The hypercarnivorous bush dog is mostly distinct in shape from all the other taxa while a degree of overlap in shape—but not size—occurs between species of the genus Lycalopex. Both climate and competition impacts interspecific morphological variation. We identified climatic adaptations as the main driving force of diversification for the South American canids. Competition has a lower degree of impact on their skull morphology although it might have played a role in the past, when canid community was richer in morphotypes.Electronic supplementary materialThe online version of this article (doi:10.1007/s11692-015-9362-3) contains supplementary material, which is available to authorized users.

Identification of novel Fgf enhancers and their role in dental evolution.

Mammalian dental morphology is under strong evolutionary pressure because of its importance for mastication and diet. While the mechanisms underlying tooth development have been widely studied in model organisms, the role of genetic regulatory elements in patterning the different elements of the occlusal surface and crown height across species is not well understood. Previous studies showed that Fibroblast Growth Factor (FGF) genes are important regulators of tooth development that influence morphological variation. We hypothesized that inter-specific variation in rodent dental morphology could be governed by nucleotide variation in genetic regulatory elements that modulate the spatial and temporal expression of the genes encoding FGF signaling molecules. In this study, we compared the variation in dental morphology across nine taxa of rodents to the variation in sequences of non-coding evolutionary conserved regions (ECRs) of Fgf3, 4, 8, 9, and 10. We correlated the variation in molar tooth cusp shape and the evolution of high molar crowns (hypsodonty) to the patterns of sequence variation in two ECRs, Fgf10ECR3, and Fgf9ECR1, respectively. By conducting luciferase and electrophoretic mobility shift assays, we determined that these ECRs could function as enhancers. These data suggest that emergence of hypsodonty and occlusal cusp patterning may have happened through the evolutionary changes in enhancers, such as Fgf9ECR1 and Fgf10ECR3, which affected the expression of major signaling molecules involved in tooth development.

First Report of Hemiclitores in Females of South American Liolaemid Lizards

Abstract Studies about copulatory organs in Squamata were restricted to the morphology of hemipenes until Bohme reported homologous paired structures in females of a species of Varanus, which he called hemiclitores. We report the presence of hemiclitores in females of Phymaturus and of two species of Liolaemus and describe observations on the interspecific variation in hemipenis morphology in Phymaturus. Phymaturus and Liolaemus belong to Liolaemidae, a species-rich family of lizards; research about hemipenis morphology is scarce and limited to a few species of those genera. We found the retractor clitoridis magnus in all of the species analyzed; however, the transverse penis was not present in all of them. The general structure of hemiclitores of Phymaturus and Liolaemus females resembled that described for other squamate species; they were smaller than hemipenes and exhibited a sulcus spermaticus. The variation found in different features of these organs (shape, size, pigmentation), as well as the gener...

Electrosensory-driven feeding behaviours of the Port Jackson shark (Heterodontus portusjacksoni) and western shovelnose ray (Aptychotrema vincentiana)

Elasmobranch fishes (sharks, skates and rays) possess a highly sensitive electrosensory system that enables them to detect weak electric fields, such as those produced by potential prey organisms. Despite several comparative anatomical studies, the functional significance of interspecific variation in electrosensory system morphology remains poorly understood. In the present study, we directly tested the electrosensitivity of two benthic elasmobranchs that share a similar habitat and feed on similarly sized prey items (Port Jackson sharks, Heterodontus portusjacksoni, and western shovelnose rays, Aptychotrema vincentiana), but differ significantly in their electrosensory system morphology. Aptychotrema vincentiana possesses almost five times the number of electrosensory pores of H. portusjacksoni (~1190 and ~239 respectively), yet both species are able to initiate feeding responses to electric-field gradients below 1 nV cm–1, similar to other elasmobranch species tested. However, A. vincentiana showed a greater ability to resolve the specific location of electrosensory stimuli, because H. portusjacksoni would more often overshoot the target and have to turn around to locate it. These results suggested that differences in abundance and distribution of electrosensory pores have little to no effect on the absolute electrical sensitivity in elasmobranchs, and instead, may reflect species-specific differences in the spatial resolution and directionality of electroreception.

The Gerbil Spermatozoon – interspecific variation in morphology does not invariably follow murine rodent evolutionary trends in response to predicted intermale sperm competition

AbstractIn various groups of mammals, the intensity of intermale sperm competition relates to relative testes mass (RTM) with some evidence suggesting that this may also be the case for some aspects of sperm form. In murid rodents, a large RTM generally correlates with a streamlined sperm head, long apical hook and long tail with most data coming from species in the subfamily Murinae. In this study, RTM and sperm form are compared across 15 species of gerbils, seven from the Tribe Taterillini and eight from the Tribe Gerbillini. Marked interspecific differences in RTM and sperm morphology were observed. However, the Gerbilliscus species with the largest RTM do not have a sperm head with an apical hook nor a longer sperm tail than other species with smaller RTM whereas, by contrast, in the Tribe Gerbillini, species where the sperm head lacks a hook have a relatively small testes mass. We thus suggest that in gerbils, unlike in murine rodents, high levels of postcopulatory sexual selection have not invariably resulted in the evolution of a spermatozoon with a long apical hook and long sperm tail. The possible reasons for this are briefly discussed.

Does claw morphology of the green crab Carcinus maenas vary in relation to its diet on rocky versus fine-sediment shores of southwest New Brunswick, Bay of Fundy, Canada?

Inter-specific variation in claw morphology of decapod crustaceans is related to the particular dietary niche different species occupy, but very few studies have investigated whether claw variation among populations of a same species is similarly related to diet. We set out to quantify differences in claw morphology between green crabs inhabiting rocky and fine-sediment shores in the southwest Bay of Fundy, Canada, and asked whether these were related to differences in the prevalence of hard- and soft-bodied prey in the crab's diet. We found that claw morphology did not differ between crabs from the two habitat types, but did significantly differ between crabs sampled from different rocky shores and different fine-sediment shores. The absence of significant differences in claw morphology between crabs from rocky and fine-sediment shores was somewhat surprising, given that we did observe significant differences in crab diet between the two habitats. However, these dietary differences were related to the prevalence of soft-bodied prey, and hard-bodied snails and mussels were the most prevalent prey items in the guts of crabs from both rocky and fine-sediment shores. Our results therefore suggest that the prevalence of soft-bodied prey in the diet of green crabs in nature does not affect the morphology of their claw. Given our findings, along with recently published patterns of phenotypic co-variance between green crab claw size and snail shell thickness, we hypothesize that consumption of hard-bodied prey may be more consequential to variation in green crab claw morphology than the diet as a whole. More field studies are needed to complement the rich tradition of lab-based research into the biochemical properties of the decapod claw, and in particular to elucidate the role of diet on intra-specific variation of this appendage in nature.