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.     

Foraging behavior and morphology: seed selection in the harvester ant genus, Pogonomyrmex

Optimally foraging animals can be behaviorally or morphologically adapted to reduce the energetic and time costs of foraging. We studied the foraging behavior and morphology of three seed harvester ant species, Pogonomyrmex barbatus, P. desertorum, and P. occidentalis, to determine the importance of behavioral strategies and morphological features associated with load carriage in reducing the costs of foraging. We found that none of five morphological features we measured had a significant impact on seed selection. Also, body size did not influence running speed, an important variable in time costs of foraging. Temperature had the largest effect on running speed in these species. Our results show that these species have foraging strategies which minimize the time costs of traveling with seeds. We also describe a pattern where the running speed in individual-foraging species is less affected by increasing seed size than in trunk-trail foragers, when temperature and body mass are held constant. These results support previous work which showed that time costs are most important in seed selection for Pogonomyrmex, and suggest that central place foraging theory may need to accommodate variation in foraging strategy to more accurately predict optimal seed size selection in harvester ants. Received: 16 June 1997 / Accepted: 15 December 1997     

Lizard scales in an adaptive radiation: variation in scale number follows climatic and structural habitat diversity in Anolis lizards

Lizard scales vary in size, shape and texture among and within species. The overall function of scales in squamates is attributed to protection against abrasion, solar radiation and water loss. We quantified scale number of Anolis lizards across a large sample of species (142 species) and examined whether this variation was related either to structural or to climatic habitat diversity. We found that species in dry environments have fewer, larger scales than species in humid environments. This is consistent with the hypothesis that scales reduce evaporative water loss through the skin. In addition, scale number varied among groups of ecomorphs and was correlated with aspects of the structural microhabitat (i.e. perch height and perch diameter). This was unexpected because ecomorph groups are based on morphological features related to locomotion in different structural microhabitats. Body scales are not likely to play an important role in locomotion in Anolis lizards. The observed variation may relate to other features of the ecomorph niche and more work is needed to understand the putative adaptive basis of these patterns. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 570–579.     

Patterns of cranial ontogeny in lacertid lizards: morphological and allometric disparity

We explored the ontogenetic dynamics of the morphological and allometric disparity in the cranium shapes of twelve lacertid lizard species. The analysed species (Darevskia praticola, Dinarolacerta mosorensis, Iberolacerta horvathi, Lacerta agilis, L. trilineata, L. viridis, Podarcis erhardii, P. melisellensis, P. muralis, P. sicula, P. taurica and Zootoca vivipara) can be classified into different ecomorphs: terrestrial lizards that inhabit vegetated habitats (habitats with lush or sparse vegetation), saxicolous and shrub‐climbing lizards. We observed that there was an overall increase in the morphological disparity (MD) during the ontogeny of the lacertid lizards. The ventral cranium, which is involved in the mechanics of jaw movement and feeding, showed higher levels of MD, an ontogenetic shift in the morphospace planes and more variable allometric patterns than more conserved dorsal crania. With respect to ecology, the allometric trajectories of the shrub‐climbing species tended to cluster together, whereas the allometric trajectories of the saxicolous species were highly dispersed. Our results indicate that the ontogenetic patterns of morphological and allometric disparity in the lacertid lizards are modified by ecology and functional constraints and that the identical mechanisms that lead to intraspecific morphological variation also produce morphological divergence at higher taxonomic levels.     

Effects of substrate color on intraspecific body color variation in the toad‐headed lizard,Phrynocephalus versicolor

Diversity in animal coloration is generally associated with adaptation to their living habitats, ranging from territorial display and sexual selection to predation or predation avoidance, and thermoregulation. However, the mechanism underlying color variation in toad‐headed Phrynocephalus lizards remains poorly understood. In this study, we investigated the population color variation of Phrynocephalus versicolor. We found that lizards distributed in dark substrate have darker dorsal coloration (melanic lizards) than populations living in light substrates. This characteristic may improve their camouflage effectiveness. A reciprocal substrate translocation experiment was conducted to clarify the potential role of morphological adaptation and physiological plasticity of this variation. Spectrometry technology and digital photography were used to quantify the color variation of the above‐mentioned melanic and nonmelanic P. versicolor populations and their native substrate. Additionally, substrate color preference in both populations was investigated with choice experiments. Our results indicate that the melanic and nonmelanic populations with remarkable habitat color difference were significantly different on measured reflectance, luminance, and RGB values. Twenty‐four hours, 30 days, and 60 days of substrate translocation treatment had little effects on dorsal color change. We also found that melanic lizards choose to live in dark substrate, while nonmelanic lizards have no preference for substrate color. In conclusion, our results support that the dorsal coloration of P. versicolor, associated with substrate color, is likely a morphological adaptation rather than phenotypic plasticity.     

Tree-based delimitation of morphologically ambiguous taxa: a study of the lizard malaria parasites on the Caribbean island of Hispaniola

Malaria parasites in the genus Plasmodium have been classified primarily on the basis of differences in morphology. These single-celled organisms often lack distinguishing morphological features, and this can encumber both species delimitation and identification. Six saurian malaria parasites have been described from the Caribbean island of Hispaniola. All six infect lizards in the genus Anolis, but only two of these parasites can be distinguished using morphology. The remaining four species overlap in morphology and geography, and cannot be consistently identified using traditional methods. We compared a morphological approach with a molecular phylogenetic approach for assessing the taxonomy of these parasites. We surveyed for blood parasites from 677 Anolis lizards, representing 26 Anolis spp. from a total of 52 sites across Hispaniola. Fifty-five of these lizards were infected with Plasmodium spp., representing several new host records, but only 24 of these infections could be matched to previously described species using traditional morphological criteria. We then estimated the phylogeny of these parasites using both mitochondrial (cytb and coxI) and nuclear (EF2) genes, and included carefully selected GenBank sequences to confirm identities for certain species. Our molecular results unambiguously corroborated our morphology-based species identifications for only the two species previously judged to be morphologically distinctive. The remaining infections fell into two well-supported and reciprocally monophyletic clades, which contained the morphological variation previously reported for all four of the morphologically ambiguous species. One of these clades was identified as Plasmodium floridense and the other as Plasmodium fairchildi hispaniolae. We elevate the latter to Plasmodium hispaniolae comb. nov. because it is polyphyletic with the mainland species Plasmodium fairchildifairchildi and we contribute additional morphological and molecular characters for future species delimitation. Our phylogenetic hypotheses indicate that two currently recognised taxa, Plasmodium minasense anolisi and Plasmodium tropiduri caribbense, are not valid on Hispaniola. These results illustrate that molecular data can improve taxonomic hypotheses in Plasmodium when reliable morphological characters are lacking.     

Testing multivariate patterns of within-island differentiation in Podarcis dugesii from Madeira

Podarcis dugesii is a polymorphic species found on the ecologically-heterogeneous Atlantic island of Madeira. Patterns of geographic variation in size-free body dimensions (body shape), scalation, and size were portrayed on maps with isophene contours. There was no dominant pattern of among-site variation as seen in several other island lizards, although some linear combinations of morphological variables showed evidence of clines towards the east coast. Multivariate statistical techniques were developed to evaluate whether morphological variation contained an ecology-related spatial pattern, after removal of the effects of statistical non-independence of studied populations. Specifically, a partial correlation matrix comparison method provided evidence to support a proposed elevation model of among-site divergence in scalation and body size, with both an alternative rainfall model and spatial non-independence held constant. Similar divergence in scalation has been observed in other lizard species on other island archipelagos as well on some continental areas. The rainfall model was rejected for both body shape and scalation. The degree of within-population polymorphism in body shape and scalation showed no clear geographic trends in general, although the elevation and rainfall models could not be rejected for female scalation.     

Pre‐ and post‐mating reproductive barriers drive divergence of five sympatric species of Naryciinae moths (Lepidoptera: Psychidae)

The biological species concept suggests that species can be separated on the basis of reproductive isolation. However, because natural interbreeding capabilities are often unknown, differences in morphology are generally used to separate species. Alternatively, genetic dissimilarity is used to separate morphologically similar species. Many genetic markers, including the maternally inherited mitochondrial cytochrome oxidase I sequence, cannot show interbreeding and therefore species status of groups may remain unresolved. In species of the genera Dahlica and Siederia (Lepidoptera: Psychidae: Naryciinae) the lack of morphological distinction and unknown interbreeding has led to unclear and unresolved taxonomic status. Mitochondrial DNA sequences suggest five sexual species to occur in Finland. However, their species status remains unconfirmed, due to a lack of knowledge on interbreeding, unclear morphological distinction and the limited variation in mitochondrial DNA. We combine three methods, a cross‐mating experiment, an analysis of mitochondrial and nuclear DNA, and a detailed male genital morphological examination, to establish the species status of the five suspected species. All suspected species exhibit intraspecies mating preference, although several interspecies pairs readily produce offspring. The genetic analysis, however, fails to show hybrids or introgression, suggesting that both pre‐ and post‐copulation mechanisms isolate the species reproductively. Morphological analysis of the male genitalia confirms that the species have diverged. Our results highlight the need of combining behavioural, morphological and genetic methods to determine species status in challenging taxonomic groups. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112 , 584–605.     

Species limits and morphometric and environmental variation within the South Andean and Patagonian Mulinum spinosum species-group (Apiaceae-Azorelloideae)

Delimiting species is an important, but frequently difficult aspect of systematics that should be addressed using data from multiple sources. Here we combine morphometric analyses and environmental characteristics to delimit species in the South Andean and Patagonian taxonomically difficult species-group composed by Mulinum spinosum, M. echinus and M. leptacanthum (Apiaceae-Azorelloideae). Molecular phylogenies have shown that these three species form part of a polytomy together with other Mulinum species, and therefore these data are not useful for their delimitation. We include measurements of 25 morphometric variables from 163 herbarium specimens and perform univariate and multivariate principal component analysis (PCA) and discriminant analysis (DA) to establish the limits amongst the three mostly sympatric, morphologically similar, and phylogenetically unresolved species. We also use 19 bioclimatic and three geographic variables from localities of the specimens to infer environmental characteristics of the taxa and test their relation with morphological variation. Morphological evidence supports the inclusion of M. echinus within the morphologically and climatically variable M. spinosum, and rejects its recognition as a distinct taxon at any rank. On the contrary, M. leptacanthum is considered a morphologically distinct species, generally restricted to high altitude areas of the southern Andes with a cooler and wetter climate. Within the widespread M. spinosum, environmental gradients of precipitation and temperature relate to morphological gradients (e.g., in leaf and inflorescence sizes, in leaf acicularity, and in fruit-wing width). These last results showed that the large morphological variation in vegetative and reproductive characteristics of this species that grows in arid and semiarid habitats are related to regional climatic gradients that have probably been important in the evolution of this species' plasticity, diversification, and differentiation.     

Reproduction and sexual dimorphism in two populations of the polymorphic spiny lizard Sceloporus minor from Hidalgo,México

Male‐biased sexual dimorphism is extensive in New World spiny lizards (Sceloporus: Phrynosomatidae) and is particularly prominent in the polymorphic minor lizard Sceloporus minor. However, the possible relationship between patterns of sexual dimorphism and gonadal development is little known for most species. In this study, we explored aspects of sexual dimorphism in noncolor morphological traits in S. minor and characterized the gonadal cycle in males and females from each of two sites (El Enzuelado and La Manzana) in Hidalgo, México, differing in key ecological aspects linked to life‐history trait expression in other lizards. Males were generally larger than females in each population and expressed larger forms of several other morphological traits, although not all comparisons attained statistical significance. Both sexes attained reproductive maturity at a larger size in El Enzuelado relative to La Manzana, and females from El Enzuelado had larger litters. Gonadal cycles differed substantially between the two populations and suggest that reproductive activity of males and females was synchronous at El Enzuelado and asynchronous at La Manzana, an unusual pattern. Geographic variation in sex‐specific responses to environmental variables may be at least partly responsible for the exceptional species diversity of spiny lizards in México.     

Numerical morphological analysis of Lettuce cultivars and species (Lactuca sect.Lactuca,Asteraceae)

L. sativa L. cultivars were compared morphologically with accessions ofL. saligna L.,L. serriola L., andL. virosa L. in order to define the infra- and interspecific variation. Multivariate analysis (principal component analysis) distinguished four groups corresponding with the four species. Infraspecific variation (e.g., colour, leaf shape) withinL. sativa is the largest, because breeding has caused a large variation in vegetative features; infraspecific variation withinL. serriola is also large. Three plants of one accession were placed betweenL. sativa andL. serriola because they showed morphological characteristics of both species. They are still classified asL. sativa. The morphological differences betweenL. sativa andL. serriola are too large to consider these two as one species. The descent of the cultivar groups and the four species is described.     

Morphological variation in Gallotia atlantica from the volcanic island of Lanzarote: subspecies designations and recent lava flows

A detailed uni‐ and multivariate analysis of within‐island geographical variation in scalation and body dimensions of the lacertid lizard, Gallotia atlantica, from Lanzarote (and two neighbouring offshore islets) was carried out. Two main morphological groupings were detected: four populations clustered within a putative malpaís group, i.e. from relatively recent volcanic lava fields (seven populations were sampled from these areas), while the other 19 populations (including the three remaining malpaís populations, and those from the offshore islets of Montaña Clara and Alegranza) also clustered together. Thus, while there is a tendency for occupation of malpaís areas to be related to morphological variation, this model does have some inconsistencies. The differentiated malpaís group comprises populations from two geographically isolated areas, one from the central‐western part of the island (Timanfaya) and the other from the north (Malpaís de la Corona). The divergence of these populations is considered to have arisen recently, rather than their being relicts of an ancient, formerly widespread, lineage. The morphological variation partially supports the previous use of two different subspecies to describe the within‐island variation. However, if such a scheme were applied then one of the subspecies would need to encompass populations from the geographically separated southern Timanfaya and Malpaís de la Corona areas, as opposed to just the latter. We reject previous observations that either malpaís individuals in general, or those corresponding to the north‐eastern subspecies, are larger than individuals from other areas. The pattern of morphological variation of G. atlantica within Lanzarote is less pronounced but shows some similarities with patterns of morphological variation in lizards from neighbouring islands. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85 , 395–406.     

Morphological variation versus genetic divergence: a taxonomic implication for Mogannia species (Cicadidae: Cicadinae)

Species showing intraspecific morphological variation tend to be very difficult to identify using morphological characters. One such example is the cicada genus Mogannia where some species show considerable intraspecific variation mainly exhibited by wing pattern and body colouration. Thirty-one variants covering different putative species of Mogannia were recognized and illustrated in the present paper. Molecular data of mitochondrial COI and Cytb sequences were employed to test the level of variation and phylogeny of them. The existence of a ‘barcoding gap’ between intraspecific and interspecific genetic divergences and the reciprocally monophyletic clades indicate that all the closely related variants represent a single species, and that all these variants correspond to six species, respectively. However, the evolutionary relationships of intraspecific variants are not resolved possibly due to insufficient genetic variation among them. Our results indicated that some morphological characters, especially the wing pattern and body colouration, and even the number of apical processes of the aedeagus in a couple of related species, must be used with great caution in delimiting Mogannia species and their relatives. The factors responsible for intraspecific morphological variation and phylogeny of Mogannia spp. are preliminarily discussed.     

Morphological correlates of ant eating in horned lizards (Phrynosoma)

The North American horned lizards ( Phrynosoma ) represent a morphologically specialized group of ant-eating lizards. Although variation in dietary fidelity is observed among the species, all appear to possess morphological specializations thought to be related to their ant-eating diets. Previous studies have examined morphological specialization in Phrynosoma , but they have not taken into account the phylogenetic relationships of its member species. In the present study, the morphological characteristics of the head, jaws and teeth that are thought to be important in prey capture and prey processing were examined to test whether variation in cranial morphology is associated with diet in lizards of the genus Phrynosoma . It is suggested that lizards of the genus Phrynosoma are indeed morphologically specialized and that ant-eating is associated with reduced dentition and an overall reduction in the robustness of morphological structures important in prey processing. Although this trend holds for the highly myrmecophagous species of Phrynosoma , a robust cranial morphology is apparent in the short-horned lizard clade ( Phrynosoma ditmarsi , Phrynosoma douglasii , Phrynosoma hernandesi , Phrynosoma orbiculare ), implying the ability to process a variety of dietary items. The present study suggests that additional feeding specializations exist within an already specialized clade (i.e. the short-horned lizard clade) and highlights the need for more detailed dietary and behavioural studies of feeding behaviour in this uniquely specialized group of lizards.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 89 , 13–24.     

Geometric morphometric and phylogenetic analyses of Arizona Sky Island populations of Scaphinotus petersi Roeschke (Coleoptera: Carabidae)

Scaphinotus petersi Roeschke, 1907 (Carabidae) is a ground beetle endemic to Sky Islands in south‐eastern Arizona. Previous taxonomic studies described several subspecies with morphological differences inhabiting geographically isolated mountain ranges. We combined molecular sequence data and morphometric data, especially head and pronotum shape analyses, to examine the variation and divergence in subspecies and isolated montane populations. In this study, we employ a combination of distance morphometrics as well as geometric morphometrics to quantify the level of morphological variation, and to test the hypothesis that geographically distinct populations of S. petersi are phenotypically distinct. Results suggest that these isolated populations have diverged morphologically and genetically. Phylogenetic analyses identified two monophyletic lineages within the species that correspond generally to pronotum shape. We observed significant morphological variation among most montane populations in of S. petersi, with the pronotum shape as the clearest delimiting trait. © 2015 The Linnean Society of London     

Morphological differentiation correlates with ecological but not with genetic divergence in a Gehyra gecko

Body size affects life history, the ecological niche of an organism and its interactions with other organisms. Resultantly, marked differences in body size between related organisms are often an indication of a species boundary. This is particularly evident in the Gehyra variegata species complex of geckos, which displays differential body sizes between genetically divergent species, but high levels of intraspecific morphological conservatism. We report on a Gehyra population that displays extraordinary body size differentiation in comparison with other G. variegata species. We used morphological and environmental data to show this population is phenotypically and ecologically distinct from its parapatric congener Gehyra lazelli and that morphology and ecology are significantly correlated. Contrastingly, mtDNA analysis indicates paraphyly between the two groups, and allele frequencies at six microsatellite loci show no population structure concordant with morpho‐/ecotype. These results suggest either ecological speciation or environmentally induced phenotypic polymorphism, in an otherwise morphologically conservative group.     

Species differentiation in the genus Chara (Charophyceae): considerable phenotypic plasticity occurs within homogenous genetic groups

Charophytes are benthic algae with a complex morphology and high phenotypic plasticity. This has led to ambiguities in species delineation. However, until now genetic studies on Chara have been based on samples collected from a restricted geographic range or only included a restricted number of taxa. This may have hindered a general interpretation of the results. We applied barcoding of matK, a rapidly evolving coding section of the plastid genome, in 324 Chara samples collected from 19 countries, in order to test whether the distribution of barcode haplotypes among individuals was consistent with species boundaries as they are currently understood. The phylogenetic tree grouped the 324 Chara individuals, which according to commonly used identification keys represented 29 species, into 12 well-defined groups (i.e. monophyletic morphospecies or groups of morphospecies). Considerable morphological variation occurred within genetically homogeneous groups. This included traits which are commonly used for Chara species determination, such as the length and number of spine cells, the length of stipulodes and bract cells, cortication (tylacanthous, isostichous, aulacanthous and absent cortication), as well as sex differentiation. However, there were also substantial genetic differences among morphologically similar species (e.g. C. virgata – C. globularis – C. connivens). No morphological trait consistently reflected genetic differences. This indicates that morphological traits for specific taxa may serve as diagnostic tools for species delimitation, but that they are not generally suitable for inferring genetic differentiation or phylogenetic relationships. We propose that (i) C. virgata and C. strigosa, (ii) C. liljebladii, C. horrida and C. baltica, and (iii) C. hispida, C. rudis and C. polyacantha are conspecific. Our data also indicate that C. gymnophylla should be divided into tylacanthous forms (which are closely related to C. contraria) and aulacanthous forms (which are related to C. vulgaris).     

Evidence for sexual isolation as a prezygotic barrier to gene flow between morphologically divergent species of Rhagoletis fruit flies

1. Certain groups of fruit flies in the genus Rhagoletis (Diptera: Tephritidae) are exemplars for sympatric speciation via host plant shifting. Flies in these species groups are morphologically similar and overlap in their geographic ranges, yet attack different, non‐overlapping sets of host plants. Ecological adaptations related to differences in host choice and preference have been shown to be important prezygotic barriers to gene flow between these taxa, as Rhagoletis flies mate on or near the fruit of their respective host plants. Non‐host‐related assortative mating is generally absent or present at low levels between these sympatrically diverging fly populations. 2. However, some Rhagoletis taxa occasionally migrate to ‘non‐natal’ plants that are the primary hosts of other, morphologically differentiated fly species in the genus. These observations raise the question of whether sexual isolation may reduce courtship and copulation between morphologically divergent species of Rhagoletis flies, contributing to their prezygotic isolation along with host‐specific mating. 3. Using reciprocal multiple‐choice mating trials, we measured sexual isolation among nine species pairs of morphologically differentiated Rhagoletis flies. Complete sexual isolation was observed in eight of the nine comparisons, while partial sexual isolation was observed in the remaining comparison. 4. We conclude that sexual isolation can be an effective prezygotic barrier to gene flow contributing to substantial reproductive isolation between many morphologically distinct Rhagoletis species, even in the absence of differential host plant choice and host‐associated mating.