scholarly journals Cryptic Patterns of Speciation in Cryptic Primates: Microendemic Mouse Lemurs and the Multispecies Coalescent

2019 ◽  
Author(s):  
Jelmer Poelstra ◽  
Jordi Salmona ◽  
George P. Tiley ◽  
Dominik Schüßler ◽  
Marina B. Blanco ◽  
...  

AbstractMouse lemurs (Microcebus) are a radiation of morphologically cryptic primates distributed throughout Madagascar for which the number of recognized species has exploded in the past two decades. This taxonomic explosion has prompted understandable concern that there has been substantial oversplitting in the mouse lemur clade. Here, we take an integrative approach to investigate species diversity in two pairs of sister lineages that occur in a region in northeastern Madagascar with high levels of microendemism and predicted habitat loss. We analyzed RADseq data with multispecies coalescent (MSC) species delimitation methods for three named species and an undescribed lineage previously identified to have divergent mtDNA. Marked differences in effective population sizes, levels of gene flow, patterns of isolation-by-distance, and species delimitation results were found among them. Whereas all tests support the recognition of the presently undescribed lineage as a separate species, the species-level distinction of two previously described species, M. mittermeieri and M. lehilahytsara is not supported – a result that is particularly striking when using the genealogical discordance index (gdi). Non-sister lineages occur sympatrically in two of the localities sampled for this study, despite an estimated divergence time of less than 1 Ma. This suggests rapid evolution of reproductive isolation in the focal lineages, and in the mouse lemur clade generally. The divergence time estimates reported here are based on the MSC and calibrated with pedigree-based mutation rates and are considerably more recent than previously published fossil-calibrated concatenated likelihood estimates, however. We discuss the possible explanations for this discrepancy, noting that there are theoretical justifications for preferring the MSC estimates in this case.

Author(s):  
Jelmer W Poelstra ◽  
Jordi Salmona ◽  
George P Tiley ◽  
Dominik Schüßler ◽  
Marina B Blanco ◽  
...  

Abstract Mouse lemurs (Microcebus) are a radiation of morphologically cryptic primates distributed throughout Madagascar for which the number of recognized species has exploded in the past two decades. This taxonomic revision has prompted understandable concern that there has been substantial oversplitting in the mouse lemur clade. Here, we investigate mouse lemur diversity in a region in northeastern Madagascar with high levels of microendemism and predicted habitat loss. We analyzed RADseq data with multispecies coalescent (MSC) species delimitation methods for two pairs of sister lineages that include three named species and an undescribed lineage previously identified to have divergent mtDNA. Marked differences in effective population sizes, levels of gene flow, patterns of isolation-by-distance, and species delimitation results were found among the two pairs of lineages. Whereas all tests support the recognition of the presently undescribed lineage as a separate species, the species-level distinction of two previously described species, M. mittermeieri and M. lehilahytsara is not supported—a result that is particularly striking when using the genealogical discordance index (gdi). Nonsister lineages occur sympatrically in two of the localities sampled for this study, despite an estimated divergence time of less than 1 Ma. This suggests rapid evolution of reproductive isolation in the focal lineages and in the mouse lemur clade generally. The divergence time estimates reported here are based on the MSC calibrated with pedigree-based mutation rates and are considerably more recent than previously published fossil-calibrated relaxed-clock estimates. We discuss the possible explanations for this discrepancy, noting that there are theoretical justifications for preferring the MSC estimates in this case. [Cryptic species; effective population size; microendemism; multispecies coalescent; speciation; species delimitation.]


PeerJ ◽  
2018 ◽  
Vol 6 ◽  
pp. e5733 ◽  
Author(s):  
Luz E. Zamudio-Beltrán ◽  
Blanca E. Hernández-Baños

Cloud forests are one of the most endangered ecosystems in the Americas, as well as one of the richest in biological diversity in the world. The species inhabiting these forests are susceptible to environmental changes and characterized by high levels of geographic structure. The Garnet-Throated Hummingbird, Lamprolaima rhami, mainly inhabits cloud forests, but can also be found in other habitats. This species has a highly restricted distribution in Mesoamerica, and five disjunct regions have been delimited within the current geographic distribution of the species from Mexico to Honduras. According to variation in size and color, three subspecies have been described: L. r. rhami restricted to the Mexican highlands and Guatemala, L. r. occidentalis distributed in Guerrero (Mexico), and L. r. saturatior, distributed in the highlands from Honduras and El Salvador. We analyzed the levels of geographic structure in L. rhami and its taxonomic implications. We used mitochondrial and nuclear DNA to analyze genetic variation, demographic history, divergence times, reconstructed a multilocus phylogeny, and performed a species delimitation analyses. We also evaluated morphological variation in 208 specimens. We found high levels of genetic differentiation in three groups, and significant variation in morphological traits corresponding with the disjunct geographic populations. L. rhami presents population stability with the highest genetic variation explained by differences between populations. Divergence time estimates suggest that L. rhami split from its sister group around 10.55 million years ago, and the diversification of the complex was dated ca. 0.207 Mya. The hypotheses tested in the species delimitation analyses validated three independent lineages corresponding to three disjunct populations. This study provides evidence of genetic and/or morphometric differentiation between populations in the L. rhami complex where four separate evolutionary lineages are supported: (1) populations from the Sierra Madre Oriental and the highlands of Oaxaca (rhami), (2) populations from the highlands of Guerrero (occidentalis), (3) populations from the highlands of Chiapas and Guatemala (this is a non-previously proposed potential taxon: tacanensis), and (4) populations from the highlands of Honduras and El Salvador (saturatior). The main promoters of the geographic structure found in the L. rhami complex are likely the Isthmus of Tehuantepec as a geographic barrier, isolation by distance resulting from habitat fragmentation, and climatic conditions during the Pleistocene.


Genes ◽  
2020 ◽  
Vol 11 (3) ◽  
pp. 293
Author(s):  
Alina Urnikytė ◽  
Alma Molytė ◽  
Erinija Pranckevičienė ◽  
Zita Aušrelė Kučinskienė ◽  
Vaidutis Kučinskas

The prehistory of the Lithuanian population and genetic relationship to other populations are poorly studied. Thus, the Lithuanian population, as an object of study, is interesting due to its partial isolation with genetic distinctiveness within the European context and with preserved ancient genetic composition. The main objects of this study was to infer demographic parameters, effective population size (Ne), and divergence time using high-density single nucleotide polymorphism (SNP) genotyping data generated with the Illumina HumanOmmiExpress-12v1.1 array in 295 individuals from the Lithuanian population and to compare our data with other populations from the Human Genome Cell Line Diversity Panel (HGDP-CEPH). We also aimed to reconstruct past events between the main ethnolinguistic regions—Aukštaitija and Žemaitija of Lithuania. Historically, these regions probably developed as two independent Baltic tribes. Our results of Ne in the Lithuanian population through time demonstrated a substantial reduction of Ne over the 150,000–25,000 years before present (YBP). The estimated long-term Ne of the Lithuanian population is quite low—it equals 5404, which likely is a consequence of the bottlenecks associated with the last glacial period of 25,000–12,000 YBP in Europe. The obtained divergence time estimates between the study populations are in agreement with recent studies. The reconstructed past events in Aukštaitija and Žemaitija showed significant differences between these two regions of Lithuania.


2019 ◽  
Author(s):  
Herman L Mays ◽  
David A Oehler ◽  
Kyle W Morrison ◽  
Ariadna E Morales ◽  
Alyssa Lycans ◽  
...  

Abstract Rockhopper penguins are delimited as 2 species, the northern rockhopper (Eudyptes moseleyi) and the southern rockhopper (Eudyptes chrysocome), with the latter comprising 2 subspecies, the western rockhopper (Eudyptes chrysocome chrysocome) and the eastern rockhopper (Eudyptes chrysocome filholi). We conducted a phylogeographic study using multilocus data from 114 individuals sampled across 12 colonies from the entire range of the northern/southern rockhopper complex to assess potential population structure, gene flow, and species limits. Bayesian and likelihood methods with nuclear and mitochondrial DNA, including model testing and heuristic approaches, support E. moseleyi and E. chrysocome as distinct species lineages with a divergence time of 0.97 Ma. However, these analyses also indicated the presence of gene flow between these species. Among southern rockhopper subspecies, we found evidence of significant gene flow and heuristic approaches to species delimitation based on the genealogical diversity index failed to delimit them as species. The best-supported population models for the southern rockhoppers were those where E. c. chrysocome and E. c. filholi were combined into a single lineage or 2 lineages with bidirectional gene flow. Additionally, we found that E. c. filholi has the highest effective population size while E. c. chrysocome showed similar effective population size to that of the endangered E. moseleyi. We suggest that the current taxonomic definitions within rockhopper penguins be upheld and that E. chrysocome populations, all found south of the subtropical front, should be treated as a single taxon with distinct management units for E. c. chrysocome and E. c. filholi.


2019 ◽  
Vol 69 (1) ◽  
pp. 184-193 ◽  
Author(s):  
E Anne Chambers ◽  
David M Hillis

AbstractMany recent species delimitation studies rely exclusively on limited analyses of genetic data analyzed under the multispecies coalescent (MSC) model, and results from these studies often are regarded as conclusive support for taxonomic changes. However, most MSC-based species delimitation methods have well-known and often unmet assumptions. Uncritical application of these genetic-based approaches (without due consideration of sampling design, the effects of a priori group designations, isolation by distance, cytoplasmic–nuclear mismatch, and population structure) can lead to over-splitting of species. Here, we argue that in many common biological scenarios, researchers must be particularly cautious regarding these limitations, especially in cases of well-studied, geographically variable, and parapatrically distributed species complexes. We consider these points with respect to a historically controversial species group, the American milksnakes (Lampropeltis triangulum complex), using genetic data from a recent analysis (Ruane et al. 2014). We show that over-reliance on the program Bayesian Phylogenetics and Phylogeography, without adequate consideration of its assumptions and of sampling limitations, resulted in over-splitting of species in this study. Several of the hypothesized species of milksnakes instead appear to represent arbitrary slices of continuous geographic clines. We conclude that the best available evidence supports three, rather than seven, species within this complex. More generally, we recommend that coalescent-based species delimitation studies incorporate thorough analyses of geographic variation and carefully examine putative contact zones among delimited species before making taxonomic changes.


Insects ◽  
2020 ◽  
Vol 11 (1) ◽  
pp. 64
Author(s):  
Sofía Muñoz-Tobar ◽  
Michael Caterino

The ant-loving beetle genus Panabachia Park 1942 is a poorly studied beetle lineage from the new world tropics. We recently collected Panabachia from several previously unrecorded locations in the páramo biome of the high Ecuadorian Andes, with males exhibiting great morphological variation in the distribution of the foveae and depressions in the pronotum, as well as aspects of the male genitalia. Here, we employ phylogenetic and species delimitation methods with mitochondrial (COI) and nuclear protein-coding (wingless) gene sequences to examine the concordance of morphological characters and geography with hypothesized species boundaries. Three methods of species delimitation (bPTP, GMYC and Stacey) were used to estimate the number of species, and divergence times between putative species using molecular clock calibration. Phylogenetic analysis revealed two parallel radiations, and species delimitation analyses suggest there are between 17 and 22 putative species. Based on clade support and concordance across species delimitation methods we hypothesize 17 distinct clusters, with allopatric speciation consistent with most geographic patterns. Additionally, a widespread species appears to be present in northern páramo sites, and some sister species sympatry may indicate other diversification processes have operated on certain lineages of Panabachia. Divergence time estimates suggest that Panabachia originated in the Miocene, but most species analyzed diverged during the Pliocene and Pleistocene (5.3–0.11 Mya), contemporaneous with the evolution of páramo plant species.


2021 ◽  
Vol 71 ◽  
pp. 781-798
Author(s):  
Gustavo Campillo-García ◽  
Oscar Flores-Villela ◽  
Brett Oliver Butler ◽  
Julián Andrés Velasco Vinasco ◽  
Fabiola Ramírez Corona

The spiny lizard genus Sceloporus was described by Wiegmann in 1828, with S. torquatus posteriorly designated as the type species. The taxonomic history of S. torquatus is complicated, as it has been confused with other taxa by numerous authors. Many modern systematics works have been published on Sceloporus, but none have included all five recognized S. torquatus subspecies: S. t. torquatus, S. t. melanogaster, S. t. binocularis, S. t. mikeprestoni, and S. t. madrensis. Additionally, there is previous evidence for at least one unnamed taxon. The present study is the first taxonomic revision of the enigmatic S. torquatus based on molecular phylogenies using combined molecular data from 12S, ND4 and RAG1 genes, and Maximum Likelihood and Bayesian inference phylogenetic methods. This work includes the most extensive sampling across the entire distribution, as well as divergence time estimates and environmental niche modelling, which combined offer a spatio-temporal framework for understanding the evolution of the species. Additionally, a series of morphological characters are analyzed to identify significant differences between lineages consistently recovered in the molecular phylogenies. Using this integrative approach, evidence is presented for eight lineages within the S. torquatus complex, five of which correspond to previously recognized subspecies and three represent unnamed taxa masked by morphological conservatism. Finally, to maintain taxonomic stability a lectotype and paralectoype are designated for S. torquatus, and certain taxonomic changes are suggested in order to reflect the phylogenetic relationships within the S. torquatus complex.


2019 ◽  
Vol 95 (1) ◽  
pp. 49-64 ◽  
Author(s):  
Felipe Polivanov Ottoni ◽  
José L. O. Mattos ◽  
Axel M. Katz ◽  
Pedro H.N. Bragança

Three distinct and independent molecular-based species delimitation analyses were performed among the species and populations included within theAustraloherosautranigroup, based on sequences of the mitochondrial gene Cytochrome b: a tree-based method proposed by Wiens and Penkrot (WP), a Character-based DNA Barcoding (CBB) and coalescent species delimitation method termed the Bayesian Implementation of the Poisson tree processes (bPTP). The congruence of WP and CBB delimited 11 independent lineages (species), while the bPTP delimited just nine lineages. We did not favour any of the methods, and we considered the possibility of two slightly variant scenarios. A time-calibrated phylogenetic analysis is proposed based on the predominant congruence of the results of these three species delimitation methods herein applied. The monophyly of theA.autranispecies group was highly supported with maximum node support value and diagnosed by 11 nucleotide substitutions. The sister clade of theA.autranispecies group is the clade comprisingA.sp. Timbé do Sul andA.minuano. The phylogenetic analysis supports three main clades within theA.autranispecies group, supported by maximum node support value, with the Southern Mata Atlântica clade as the most basal clade. Divergence time estimates indicate that the diversification of theAustraloherosoriginated during the early Neogene, but only in the late Neogene did the processes of diversification in the southeast and north regions occur. Diversification within theAustraloherosautranispecies group occurred synchronically for the three main clades during the beginning of the Quaternary. It is demonstrated that molecular characters are valuable tools for species recognition, particularly in speciose groups with inconspicuous or difficult to record morphological characters. The resulting phylogeny of theAustraloherosautranigroup is highly compatible with the geological and biogeographic scenarios proposed for the Neogene and Quarternary shaping of the extant river basins of eastern Brazil. Despite the origin of theA.autranigroup being dated to the late Miocene, species level diversification occurred in the Pleistocene and was probably driven by headwater capture events and sea-level fluctuations.


PeerJ ◽  
2017 ◽  
Vol 5 ◽  
pp. e3724 ◽  
Author(s):  
Ana C. Afonso Silva ◽  
Natali Santos ◽  
Huw A. Ogilvie ◽  
Craig Moritz

While methods for genetic species delimitation have noticeably improved in the last decade, this remains a work in progress. Ideally, model based approaches should be applied and considered jointly with other lines of evidence, primarily morphology and geography, in an integrative taxonomy framework. Deep phylogeographic divergences have been reported for several species ofCarliaskinks, but only for some eastern taxa have species boundaries been formally tested. The present study does this and revises the taxonomy for two species from northern Australia,Carlia johnstoneiandC. triacantha. We introduce an approach that is based on the recently published method StarBEAST2, which uses multilocus data to explore the support for alternative species delimitation hypotheses using Bayes Factors (BFD). We apply this method, jointly with two other multispecies coalescent methods, using an extensive (from 2,163 exons) data set along with measures of 11 morphological characters. We use this integrated approach to evaluate two new candidate species previously revealed in phylogeographic analyses of rainbow skinks (genusCarlia) in Western Australia. The results based on BFD StarBEAST2, BFD* SNAPP and BPP genetic delimitation, together with morphology, support each of the four recently identifiedCarlialineages as separate species. The BFD StarBEAST2 approach yielded results highly congruent with those from BFD* SNAPP and BPP. This supports use of the robust multilocus multispecies coalescent StarBEAST2 method for species delimitation, which does not requirea prioriresolved species or gene trees. Compared to the situation inC. triacantha, morphological divergence was greater between the two lineages within Kimberley endemicC. johnstonei, which also had deeper divergent histories. This congruence supports recognition of two species withinC. johnstonei. Nevertheless, the combined evidence also supports recognition of two taxa within the more widespreadC. triacantha. With this work, we describe two new species,Carlia insularissp. nov andCarlia isostriacanthasp. nov. in the northwest of Australia. This contributes to increasing recognition that this region of tropical Australia has a rich and unique fauna.


Author(s):  
Maysa T Motoki ◽  
Yvonne-Marie Linton ◽  
Jan E Conn ◽  
Fredy Ruiz-Lopez ◽  
Richard C Wilkerson

Abstract The Neotropical Albitarsis Group is a complex assemblage of essentially isomorphic species which currently comprises eight recognized species—five formally described (Anopheles albitarsis Lynch-Arribalzaga, An. deaneorum Rosa-Freitas, An. janconnae Wilkerson and Sallum, An. marajoara Galvao and Damasceno, An. oryzalimnetes Wilkerson and Motoki) and three molecularly assigned (An. albitarsis F, G & I)—and one mitochondrial lineage (An. albitarsis H). To further explore species recognition within this important group, 658 base pairs of the mitochondrial DNA cytochrome oxidase subunit I (COI) were analyzed from 988 specimens from South America. We conducted statistical parsimony network analysis, generated estimates of haplotype, nucleotide, genetic differentiation, divergence time, and tested the effect of isolation by distance (IBD). Ten clusters were identified, which confirmed the validity of the eight previously determined species, and confirmed the specific status of the previous mitochondrial lineage An. albitarsis H. High levels of diversity were highlighted in two samples from Pará (= An. albitarsis J), which needs further exploration through additional sampling, but which may indicate another cryptic species. The highest intra-specific nucleotide diversity was observed in An. deaneorum, and the lowest in An. marajoara. Significant correlation between genetic and geographical distance was observed only in An. oryzalimnetes and An. albitarsis F. Divergence time within the Albitarsis Group was estimated at 0.58–2.25 Mya, during the Pleistocene. The COI barcode region was considered an effective marker for species recognition within the Albitarsis Group and a network approach was an analytical method to discriminate among species of this group.


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