Sympatric Clades Research Articles

Species richness under a vertebral stripe: integrative taxonomy uncovers three additional species of Pholidobolus lizards (Sauria, Squamata, Gymnophthalmidae) from the north-western Colombian Andes.

The systematic study of biodiversity underlies appropriate inference in most other fields of biological research, yet it remains hampered by disagreements on both theoretical and empirical issues such as the species concept and the operational diagnosis of a species. Both become particularly challenging in those lineages where morphological traits are evolutionarily constrained by their adaptive value. For instance, cryptic organisms often conserve or converge in their external appearance, which hinders the recognition of species boundaries. An integrative approach has been adopted to study microgeographic variation in the leaf-litter lizard Pholidobolusvertebralis and test three predictions derived from the evolutionary species concept. Molecular data provided unambiguous evidence of divergence among the three recovered new clades and a common evolutionary history for each of them. The broadly sympatric clades were indeed diagnosable from externally visible traits, such as head scales, adult size, and sexually dimorphic ventral colouration. Also, they barely overlapped on the phenotypic space that summarised 39 morphometric and meristic traits. These clades are described as three species and an available name is suggested for a recovered fourth clade. The geographic distribution of the new and proximate species suggests a role for elevation on evolutionary divergence; it also raises interesting questions on the speciation pattern of an otherwise underestimated cryptic lineage.

Disentangling the Impacts of Speciation, Sympatry and the Island Effect on the Morphology of Seven Hynobius sp. Salamanders.

Closely related individuals from different areas can see their morphologies change based on differences between clades, but also ecological variables such as the island effect or sympatry. This is the case of salamanders, which have adapted to a broad range of ecological niches, ranging from underground dwellers in xeric landscape to tropical arboreal habitats. On the Korean Peninsula, salamanders from the Hynobius clade are widespread on the mainland and islands, with several partially sympatric clades and candidate species. Currently, seven lineages have been identified based on mtDNA, four of them matching named species and three others for which the species status remains untested. While the morphology of Korean Hynobius is known to be variable between genetically segregated clades, we hypothesise that (1) the candidate species are morphologically different, and that (2) the island effect and (3) the sympatric status have significant impacts on the morphology of individuals within the genus. Here we measured 329 Hynobius salamanders from all seven clades, in areas of sympatry and allopatry, and on islands and on the mainland (Graphical Abstract A). We determined that the island effect had a significant impact on the morphology of the genus, with mainland individuals generally displaying a broader range of morphology than islandic individuals (Graphical Abstract B). We also determined that sympatry had an impact on morphology, with the sizes of individuals from clades in sympatric areas diverging from each other (Graphical Abstract C). Finally, we demonstrated that all seven clades have significantly different morphologies, and we described the three candidate species that had already been isolated based on mtDNA and microsatellite data: Hynobius notialis sp. nov., Hynobius geojeensis sp. nov. and Hynobius perplicatus sp. nov. We conclude that looking at morphology alone would be misleading about the true diversity of Hynobius species, and species in general, because of the island and patry effects.

Dietary morphology of two island-endemic murid rodent clades is consistent with persistent, incumbent-imposed competitive interactions.

A lineage colonizing a geographic region with no competitors may exhibit rapid diversification due to greater ecological opportunity. The resultant species diversity of this primary-colonizing (incumbent) clade may limit subsequent lineages' ability to persist unless these non-incumbent lineages are ecologically distinct. We compare the diversity in diet-related mandibular morphology of two sympatric murid rodent clades endemic to Luzon Island, Philippines-incumbent Phloeomyini and secondary-colonizing Chrotomyini-to the mandibular morphological diversity of Sahul Hydromyini, the sister clade of Chrotomyini and the incumbent murid lineage on the supercontinent of Sahul. This three-clade comparison allows us to test the hypothesis that incumbent lineages can force persistent ecological distinction of subsequent colonists at the time of colonization and throughout the subsequent history of the two sympatric clades. We find that Chrotomyini forms a subset of the diversity of their clade plus Sahul Hydromyini that minimizes overlap with Phloeomyini. We also infer that this differentiation extends to the stem ancestor of Chrotomyini and Sahul Hydromyini, consistent with a biotic filter imposed by Phloeomyini. Our work illustrates that incumbency has the potential to have a profound influence on the ecomorphological diversity of colonizing lineages at the island scale even when the traits in question are evolving at similar rates among independently colonizing clades.

Spiny trapdoor spiders (Euoplos) of eastern Australia: Broadly sympatric clades are differentiated by burrow architecture and male morphology

Spiders of the infraorder Mygalomorphae are fast becoming model organisms for the study of biogeography and speciation. However, these spiders can be difficult to study in the absence of fundamental life history information. In particular, their cryptic nature hinders comprehensive sampling, and linking males with conspecific females can be challenging. Recently discovered differences in burrow entrance architecture and male morphology indicated that these challenges may have impeded our understanding of the trapdoor spider genus Euoplos in Australia’s eastern mesic zone. We investigated the evolutionary significance of these discoveries using a multi-locus phylogenetic approach. Our results revealed the existence of a second, previously undocumented, lineage of Euoplos in the eastern mesic zone. This new lineage occurs in sympatry with a lineage previously known from the region, and the two are consistently divergent in their burrow entrance architecture and male morphology, revealing the suitability of these characters for use in phylogenetic studies. Divergent burrow entrance architecture and observed differences in microhabitat preferences are suggested to facilitate sympatry and syntopy between the lineages. Finally, by investigating male morphology and plotting it onto the phylogeny, we revealed that the majority of Euoplos species remain undescribed, and that males of an unnamed species from the newly discovered lineage had historically been linked, erroneously, to a described species from the opposite lineage. This paper clarifies the evolutionary relationships underlying life history diversity in the Euoplos of eastern Australia, and provides a foundation for urgently needed taxonomic revision of this genus.

Extensive genetic diversity and endemism across the global range of the oceanic copepod Pleuromamma abdominalis

Many oceanic zooplankton species have been described as cosmopolitan in distribution; however, recent molecular work has detected species complexity with highly divergent genetic lineages within several of these taxa. To further resolve the species complexity within these ecologically-important and widespread species, we performed both molecular and morphological analyses of the oceanic copepod Pleuromamma abdominalis using a comprehensive collection of material from 944 individuals collected at 46 sites across the global ocean. Phylogenetic analyses of mitochondrial cytochrome oxidase subunit I (mtCOI) sequences detected eighteen divergent evolutionary lineages within P. abdominalis, with an additional four singleton specimens that were also genetically divergent. Two phylogenetically distinct groups, PLAB1 and PLAB2, were supported by concordant sequence variation in the nuclear large subunit ribosomal RNA gene (nLSU). Within PLAB1, two mtCOI clades, 1a-1 and 1b-1 were observed, and each clade contained geographically distinct sub-clades 1a-2 and 1b-2. PLAB2 was composed of sixteen well-supported mtCOI clades (2a–2p) as well as four singletons. High genetic divergence among the mtCOI lineages within both PLAB1 and PLAB2, ranging between 9.2–11.2% and 4.3–18.9% K2P distances respectively, suggests the presence of additional species within these groups. Significant differences were observed in the presence and shape of antennule spines of adult females between sympatric clades with genetic distances greater than 5.7–7.0% (K2P). The biogeographic distributions of mtCOI clades indicated greater specialization to particular oceanographic provinces than observed in the nominal species P. abdominalis, with mtCOI clades ranging from antitropical in subtropical waters of all three ocean basins (Atlantic, Pacific and Indian; clade 1b-1 and 2a) to taxa that are endemic to a particular ocean region, for example restricted to equatorial waters of the Atlantic Ocean (clade 1b-2 and 2b). We hypothesize that many of these mtCOI clades are likely distinct, and currently undescribed species. The well-known high dominance of P. abdominalis across a range of pelagic habitats may occur as a spatial composite of genetically-distinct species with more restricted distributions and greater ecological specialization to particular marine habitats than was previously recognized.

Terrestrial fishes: rivers are barriers to gene flow in annual fishes from the African savanna

AbstractAimWe compared the genetic variability and phylogeographical structure of three sympatric clades of annual killifishes (the Nothobranchius furzeri complex, N. orthonotus complex and N. rachovii complex) inhabiting annually desiccating savanna pools. Hypotheses on the mechanisms affecting intraspecific structure and speciation were tested.LocationTemporary pools in Mozambique (Africa).MethodsThe study is based on spatially detailed samples covering the entire range of all three species complexes. A set of 12–13 microsatellites (1638 individuals, 96 populations) and cytochrome b sequences (463 fish, 152 populations) were used as genetic markers. Phylogenetic and population genetic approaches were used to describe the spatial genetic structure and to test the respective roles of river channels and river basins on diversification.ResultsProfound genetic differentiation among populations was evident; some populations located only a few kilometres apart were genetically very distinct, suggesting a significant role of genetic drift and low dispersal ability. Large rivers (Zambezi, Save, Limpopo) formed major barriers to gene flow, with minor differences among the three complexes. Further, the demographic expansion of previously isolated lineages was often limited by the river channel, and rivers were also confirmed as factors affecting speciation events. River basins and elevational gradient had a smaller, but non‐negligible, role in population structuring.Main conclusionsRiver channels are the main barriers to gene flow in Nothobranchius fishes. The study demonstrated low dispersal ability and congruence in the phylogeographical pattern of all three complexes. Cases where Nothobranchius appear to have crossed river channels result from the dynamics of river morphology rather than from rare dispersal events. This conclusion is supported by simultaneous crossing events across lineages. A further division, also consistent among the three complexes, was detected between drier inland and wetter coastal areas. The phylogeographical pattern of Nothobranchius is unique in that it combines features of both aquatic and terrestrial taxa.

Large Spatial Scale of the Phenotype-Environment Color Matching in Two Cryptic Species of African Desert Jerboas (Dipodidae: Jaculus)

We tested the camouflage hypothesis, or the linkage between animal (Saharan rodent) and habitat coloration, on the largest geographical scale yet conducted. We aimed to determine whether phenotypic variation is explained by micro-habitat variation and/or genetic polymorphism to determine 1) the strength of linkage between fur color and local substrate color, and 2) the divergence in fur coloration between two genetic clades, representing cryptic species, throughout the complete range of the African desert jerboas (Jaculus jaculus). We used a combination of museum and field-collected specimens, remote sensing tools, satellite and digital photography and molecular genetic and phylogenetic methods to investigate the above hypotheses. Along with showing that the two divergent genetic clades of jerboas occur sympatrically throughout their African distribution, we showed significant covariation between dorsal fur coloration of the animals and the color of their habitat. We also described significant phenotypic divergence in fur color, consistent with genetic divergence between the sympatric clades. The linkage between environment and phenotype supports the idea that the selection promoting cryptic coloration is persistent in contemporary populations of jerboas, however the phenotypic divergence indicates that it has different strengths (or optima) in the two clades. The mosaic distribution of micro-habitats occupied by geographically sympatric clades suggests that it may influence both ecological and evolutionary dynamics between these two cryptic species.

Cryptic diversity within and amongst spring-associatedStygobromusamphipods (Amphipoda: Crangonyctidae)

Multiple species of troglomorphic, spring-associated Stygobromus amphipods, including the endangered, narrow-range endemic Stygobromus pecki, occupy sites in the Edwards Plateau region of North America. Given the prevalence of cryptic diversity observed in disparate subterranean, animal taxa, we evaluated geographical genetic variation and tested whether Stygobromus contained undetected biodiversity. Nominal Stygobromus taxa were treated as hypotheses and tested with mitochondrial sequence cytochrome oxidase C subunit 1, nuclear sequence (internal transcribed spacer region 1), and AFLP data. Stygobromus pecki population structure and diversity was characterized and compared with congeners. For several Stygobromus species, the nominal taxonomy conflicted with molecular genetic data and there was strong evidence of significant cryptic diversity. Whereas S. pecki genetic diversity was similar to that of congeners, mitochondrial data identified two significantly diverged but sympatric clades. AFLP data for S. pecki indicated relatively recent and ongoing gene flow in the nuclear genome. These data for S. pecki suggest either a substantial history of isolation followed by current sympatry and ongoing admixture, or a protracted period of extremely large effective population size. This study demonstrates that Edwards Plateau Stygobromus are a complex, genetically diverse group with substantially more diversity than currently recognized. © 2013 The Linnean Society of London

Cryptic lineages of little free-tailed bats, Chaerephon pumilus (Chiroptera: Molossidae) from southern Africa and the western Indian Ocean islands

We investigate mitochondrial DNA and craniometric variation in southern African and Malagasy populations of the small and morphologically variable, house-roosting molossid bat, Chaerephon pumilus in relation to Malagasy populations of the related, smaller-sized species, C. leucogaster. Both cytochrome b and D-loop sequences show C. leucogaster to be nested within C. pumilus sensu lato, with Malagasy C. pumilus forming a sister group to African C. pumilus and Malagasy C. leucogaster. Four distinct D-loop clades are found in southern African populations, all of which occur sympatrically in the greater Durban area of KwaZulu-Natal Province, whilst two of the Durban clades also characterize 1) northern KwaZulu-Natal and low-lying (<600 m) areas of Swaziland, and 2) ‘inland’ populations comprising the Kruger National Park and higher-lying (>600 m) areas of Swaziland. Clades from low-lying areas show evidence of historical demographic expansion around 3300–13 000 years ago (KwaZulu-Natal coastal clade, Clade A1) to 14 700–60 000 years ago (Durban clade, Clade B1), whilst the inland clade (Clade B2a) was demographically more stable. The origin of these clades can be explained by sea level and vegetation changes hypothesized to follow the Last Glacial Maximum (LGM) after 18 000 years ago. Sympatric clades are shown to differ significantly in the proportional width of the braincase, and ongoing work will test evidence for acoustic and other morphological differences between them.

CAN PARALLEL DIVERSIFICATION OCCUR IN SYMPATRY? REPEATED PATTERNS OF BODY-SIZE EVOLUTION IN COEXISTING CLADES OF NORTH AMERICAN SALAMANDERS

A classic paradigm in evolutionary biology is that geographically isolated clades inhabiting similar selective regimes will diversify to create similar sets of phenotypes in different locations (e.g., similar stickleback species in different lakes, similar Anolis ecomorphs on different islands). Such parallel radiations are not generally expected to occur in sympatry because the available niche space would be filled by whichever clade is diversified first. Here, we document a very different pattern, the parallel evolution of similar body-size morphs in three sympatric clades of plethodontid salamanders (Desmognathus, Plethodon, Spelerpinae) in eastern North America. Using a comprehensive, time-calibrated phylogeny of North American plethodontids from nuclear and mitochondrial DNA sequences, we show that these three clades have undergone replicated patterns of evolution in body size and that this parallel diversification occurred in broad-scale sympatry. At the local scale, we find that coexisting species from these clades are more similar in body size than expected under a null model in which species are randomly assembled into communities. These patterns are particularly surprising in that competition is known to be important in driving phenotypic diversification and limiting local coexistence of similar-sized species within these clades. Although parallel diversification of sympatric clades may seem counterintuitive, we discuss several ecological and evolutionary factors that may allow the phenomenon to occur.

Continental speciation in the tropics: contrasting biogeographic patterns of divergence in theUroplatusleaf‐tailed gecko radiation of Madagascar

AbstractA fundamental expectation of vicariance biogeography is for contemporary cladogenesis to produce spatial congruence between speciating sympatric clades. TheUroplatusleaf‐tailed geckos represent one of most spectacular reptile radiations endemic to the continental island of Madagascar, and thus serve as an excellent group for examining patterns of continental speciation within this large and comparatively isolated tropical system. Here we present the first phylogeny that includes complete taxonomic sampling for the group, and is based on morphology and molecular (mitochondrial and nuclear DNA) data. This study includes all described species, and we also include data for eight new species. We find novel outgroup relationships forUroplatusand find strongest support forParoeduraas its sister taxon.Uroplatusis estimated to have initially diverged during the mid‐Tertiary in Madagascar, and includes two major speciose radiations exhibiting extensive spatial overlap and estimated contemporary periods of speciation. All sister species are either allopatric or parapatric. However, we found no evidence for biogeographic congruence between these sympatric clades, and dispersal events are prevalent in the dispersal–vicariance biogeographic analyses, which we estimate to date to the Miocene. One sister‐species pair exhibits isolated distributions that we interpret as biogeographic relicts, and two sister‐species pairs have parapatric distributions separated by elevation. Integrating ecological niche models with our phylogenetic results finds both conserved and divergent niches between sister species. We also found substantial intra‐specific genetic variation, and for the three most widespread species, poor intra‐specific predictive performance for ecological niche models across the latitudinal span of Madagascar. These latter results indicate the potential for intra‐specific niche specialization along environmental gradients, and more generally, this study suggests a complex speciation history for this group in Madagascar, which appears to include multiple speciation processes.

THE GEOGRAPHICAL PATTERN OF SPECIATION AND FLORAL DIVERSIFICATION IN THE NEOTROPICS: THE TRIBE SINNINGIEAE (GESNERIACEAE) AS A CASE STUDY

The geographical pattern of speciation and the relationship between floral variation and species ranges were investigated in the tribe Sinningieae (Gesneriaceae), which is found mainly in the Atlantic forests of Brazil. Geographical distribution data recorded on a grid system of 0.5 x 0.5 degree intervals and a near-complete species-level phylogenetic tree of Sinningieae inferred from a simultaneous analysis of seven DNA regions were used to address the role of geographical isolation in speciation. Geographical range overlaps between sister lineages were measured across all nodes in the phylogenetic tree and analyzed in relation to relative ages estimated from branch lengths. Although there are several cases of species sympatry in Sinningieae, patterns of sympatry between sister taxa support the predominance of allopatric speciation. The pattern of sympatry between sister taxa is consistent with range shifts following allopatric speciation, except in one clade, in which the overlapping distribution of recent sister species indicates speciation within a restricted geographical area and involving changes in pollinators and habitats. The relationship between floral divergence and regional sympatry was also examined by analyzing floral contrasts, phenological overlap, and the degree of sympatry between sister clades. Morphological contrast between flowers is not increased in sympatry and phenological divergence is more apparent between allopatric clades than between sympatric clades. Therefore, our results failed to indicate a tendency for sympatric taxa to minimize morphological and phenological overlap (geographic exclusion and/or character displacement hypotheses). Instead, they point toward adaptation in phenology to local conditions and buildup of sympatries at random with respect to flower morphology. Additional studies at a lower geographical scale are needed to identify truely coexisting species and the components of their reproductive isolation.

Caribbean Placozoan Phylogeography

We here address placozoan distribution and phylogeography in five locations in the Caribbean Sea. We performed a coarse-resolution presence/absence survey of placozoans in Belize, Bermuda, Grenada, Jamaica, and Panama and a fine-resolution study of the distribution of placozoans in Twin Cays, Belize. Placozoans were recovered in every country sampled. Animals were sequenced at the mitochondrial 16S rDNA locus, and our analysis identified four of the five previously identified clades present in the Caribbean. In addition, we discovered two new haplotypes within one of these clades, and we found sympatric clades in Belize, Bermuda, Jamaica, and Panama. These studies provide further molecular evidence for species diversity within the Phylum Placozoa.

The effects of mode of development on phylogeography and population structure of North Atlantic Crepidula (Gastropoda: Calyptraeidae).

The mode of development of marine invertebrates is thought to influence levels of population structure and the location of species range endpoints via differences in dispersal ability. To examine these effects, populations of three sympatric clades of sedentary, marine gastropods in the genus Crepidula were sampled along the Atlantic and Gulf coasts of North America. A haplotype tree was constructed for each clade based on 640 bp sequences of mitochondrial cytochrome oxidase c subunit I. Examination of the tree topology, and AMOVA analysis show that species with direct development (those hatching as benthic juveniles) have higher levels of population structure than do species with planktonic development. Both species in the direct-developing C. convexa clade have high levels of geographical differentiation, with most populations representing a discrete clade of haplotypes. The planktotrophic species C. fornicata contains two major haplotype clades, both of which include samples from throughout the Atlantic coast. In this species there is no geographical differentiation among haplotypes but AMOVA analysis detects a small but statistically significant level of geographical structure. The population structure within the C. plana species complex appears also to vary with mode of development: C. atrasolea, a direct-developing species, has higher levels of population structure than does C. depressa, a sympatric planktotrophic species. The coincident occurrence of range endpoints and genetic breaks along the east coast of Florida in both direct-developing species and species with planktonic development indicates that this biogeographic break is not due to development-specific mechanisms such as hydrographic effects on larval recruitment.