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Minimum-spanning network for T. francoisi, T. leucocephalus and T. poliocephalus haplotypes. Each circle represents a haplotype and the diameter scales to haplotype frequency. Mutational steps are represented by black dots on lines connecting haplotypes. Sampling lots are presented as colored circles. doi:10.1371/journal.pone.0061659.g004
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To understand the evolutionary processes leading to the diversity of Asian colobines, we report here on a phylogenetic, phylogeographical and population genetic analysis of three closely related langurs, Trachypithecus francoisi, T. poliocephalus and T. leucocephalus, which are all characterized by different pelage coloration predominantly on the h...
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Context 1
... of T. leucocephalus (W01-W12) and T. poliocephalus (G01-G03) formed monophyletic clades, which were nested within a polyphyletic T. francoisi (B01-B29) clade. The network shows a similar pattern (Figure 4). According to Bayesian divergence age estimations, T. leucocephalus and T. poliocephalus separated from T. francoisi populations 0.46-0.27 ...
Citations
... In this study, we sequenced a 393 bp fragment of the mtDNA D-loop from 23 captive T. francoisi from European zoos, using samples previously collected and stored by zoos and museums (see Supplementary Material for details). Combined with 42 sequences previously published by Liu et al. (2013) from 29 wild T. francoisi, 12 T. leucocephalus, and 3 T. poliocephalus, we produced a multiple alignment showing 96 polymorphic sites. Pair-wise sequence difference ranged from 0% to 6.8%, with a mean of 3.4%. ...
... Pair-wise sequence difference ranged from 0% to 6.8%, with a mean of 3.4%. We designed the sampling of captive individuals of T. francoisi to maximise the number of matrilines sequenced and included almost all known matrilines in European zoos, this is reflected in a high haplotype diversity (h) (0.925 ± 0.001), similar to that in wild populations of this species, while nucleotide diversity (π) was slightly lower (0.026 ± 0.0002) than in wild animals (Liu et al., 2013). ...
... Only one of the haplotypes from EEP animals has previously been reported from wild populations, while the remaining 11 haplotypes are newly reported. This suggests that either not all extant wild haplotypes were sampled by Liu et al. (2013) or that some wild haplotypes became extinct prior to the sampling of the wild populations. ...
Assessing the genetic diversity of captive populations of endangered species is key to the successful management of conservation-breeding programs. In this study, we sequenced a 393-bp fragment of the mitochondrial DNA (mtDNA) control region of 23 captive individuals of the Endangered François’ langur ( Trachypithecus francoisi ) to assess the mtDNA diversity of the European captive population and to identify the possible geographical origins of the population founders. Combined with 42 sequences previously published from 29 wild François’ langurs, we identified a total of 40 haplotypes in T. francoisi , including 12 haplotypes in the 23 samples from the European captive population. Only one of the haplotypes from captive animals has previously been reported from wild populations; the remaining 11 haplotypes are newly reported here. Our results suggest that the captive T. francoisi population currently holds a relatively good genetic diversity compared with many other captive populations, that this diversity originates from a fairly broad range across the species’ distribution in the wild, and that the captive population could play a significant role in increasing genetic diversity of isolated wild populations. However, the European captive population is currently quite small, and genetic diversity could be lost rapidly, which has been demonstrated in other captive populations. We recommend further investigation of the genetic diversity of captive and wild T. francoisi populations, as well as the effective conservation of this diversity.
... At present, 20 species of Trachypithecus are recognized (Anandam et al., 2013;Roos, 2021;Roos et al., 2014Roos et al., , 2019aRowe & Myers, 2016, Zinner et al., 2013, but until recently, different classifications with generally lower species numbers and varying species assemblies have been proposed (Brandon-Jones, 1984, 1995, 1996Brandon-Jones et al., 2004;Groves, 2001;Napier, 1985;Napier & Napier, 1967Oates et al., 1994;Roos et al., 2007;Weitzel & Groves, 1985). With increasing knowledge, particularly from genetic studies, a clearer picture of the evolutionary history of these primates has been obtained, which has also informed taxonomic revisions of the genus (Geissmann et al., 2004;He et al., 2012;Karanth, 2008Karanth, , 2010Karanth et al., 2008;Liedigk et al., 2009;Liu et al., 2013Liu et al., , 2020Nadler et al., 2005;Osterholz et al., 2008;Perelman et al., 2011;Roos & Zinner, 2021;Roos et al., 2007Roos et al., , 2008Roos et al., , 2019aThant et al., 2013;Wang et al., 2012Wang et al., , 2015Wangchuk et al., 2008;Zhang & Ryder, 1998). ...
... crepusculus), however, studies indicate that it is likely of hybrid origin (Liedigk et al., 2009;Roos et al., 2019a). Although various phylogenetic studies on Trachypithecus are available, they are generally limited to only a few species or individual species groups, or are based on short sequences of mitochondrial or nuclear DNA (Geissmann et al., 2004;He et al., 2012;Karanth, 2008Karanth, , 2010Karanth et al., 2008;Liedigk et al., 2009;Liu et al., 2013Liu et al., , 2020Nadler et al., 2005;Osterholz et al., 2008;Perelman et al., 2011;Roos et al., 2007Roos et al., , 2008Roos et al., , 2019aThant et al., 2013;Wang et al., 2012Wang et al., , 2015Wangchuk et al., 2008;Zhang & Ryder, 1998). Thus, a well-supported and complete species-level phylogeny for the genus is still missing. ...
... In the current study, we inferred a robust mitochondrial species-level phylogeny of the genus Trachypithecus. In contrast to earlier studies, which examined only fragments of the mitogenome and/or a few species (Geissmann et al., 2004;He et al., 2012;Karanth, 2008Karanth, , 2010Karanth et al., 2008;Liedigk et al., 2009;Liu et al., 2013;Nadler et al., 2005;Osterholz et al., 2008;Roos et al., 2007Roos et al., , 2008Thant et al., 2013;Wang et al., 2012Wang et al., , 2015Wangchuk et al., 2008;Zhang & Ryder, 1998), we included full-length mitogenomes of all 20 currently recognized species (Anandam et al., 2013;Roos, 2021;Roos et al., 2014;Rowe & Myers, 2016;Zinner et al., 2013), including two name-bearing types. Based on this dataset, we resolved the branching patterns among and within species groups, except for the radiation within T. phayrei, with strong nodal support. ...
Trachypithecus, which currently contains 20 species divided into four groups, is the most speciose and geographically dispersed genus among Asian colobines. Despite several morphological and molecular studies, however, its evolutionary history and phylogeography remain poorly understood. Phayre's langur (Trachypithecus phayrei) is one of the most widespread members of the genus, but details on its actual distribution and intraspecific taxonomy are limited and controversial. Thus, to elucidate the evolutionary history of Trachypithecus and to clarify the intraspecific taxonomy and distribution of T. phayrei, we sequenced 41 mitochondrial genomes from georeferenced fecal samples and museum specimens, including two holotypes. Phylogenetic analyses revealed a robustly supported phylogeny of Trachypithecus, suggesting that the T. pileatus group branched first, followed by the T. francoisi group, and the T. cristatus and T. obscurus groups most recently. The four species groups diverged from each other 4.5-3.1 million years ago (Ma), while speciation events within these groups occurred much more recently (1.6-0.3 Ma). Within T. phayrei, we found three clades that diverged 1.0-0.9 Ma, indicating the existence of three rather than two taxa. Following the phylogenetic species concept and based on genetic, morphological, and ecological differences, we elevate the T. phayrei subspecies to species level, describe a new species from central Myanmar, and refine the distribution of the three taxa. Overall, our study highlights the importance of museum specimens and provides new insights not only into the evolutionary history of T. phayrei but the entire Trachypithecus genus as well.
... First, the shallow evolutionary history of the species may have restricted the accumulation of population genetic variations. Mitochondrial sequence analysis showed that the WHL forms a monophyletic clade within Franc is's langurs (Trachypithecus francoisi) and that it split from the latter 0.46-0.27 million years ago [63]. These 2 species currently inhabit adjacent ranges separated by rivers and other geographic barriers and seem to represent a typical case of peripatric speciation [69]. ...
Background:
Current patterns of population genetic variation may have been shaped by long-term evolutionary history and contemporary demographic processes. Understanding the underlying mechanisms that yield those patterns is crucial for informed conservation of endangered species. The critically endangered white-headed langur, Trachypithecus leucocephalus, is endemic to a narrow range in southwest China. This species shows very low genetic diversity in its 2 main relict populations, Fusui and Chongzuo. Whether this has been caused by a short evolutionary history or recent population declines is unknown. Therefore, we investigated the contributions of historical and recent population demographic changes to population genetic diversity by using 15 nuclear microsatellite markers and mitochondrial DNA (mtDNA) control region sequences.
Results:
Using genetic data from 214 individuals we found a total of 9 mtDNA haplotypes in the Fusui population but only 1 haplotype in the Chongzuo population, and we found an overall low genetic diversity (haplotype and nucleotide diversities: h = 0.486 ± 0.036; π = 0.0028 ± 0.0003). The demographic history inferred from mtDNA and microsatellite markers revealed no evidence for historical population size fluctuations or recent population bottlenecks. Simulations of possible population divergence histories inferred by DIYABC analysis supported a recent divergence of the Chongzuo population from the Fusui population and no population bottlenecks.
Conclusions:
Despite severe population declines caused by anthropogenic activities in the last century, the low genetic diversity of the extant white-headed langur populations is most likely primarily due to the species' shallow evolutionary history and to a recent, local population founder event.
... This marker is rapidly evolving in vertebrates and thus suitable to studying events that took place during the Pliocene-Pleistocene period (Mekonnen et al. 2018). Control regions have been used widely in investigating phylogenetics, phylogeography and population genetics in primates across wide taxa such as gibbons, langurs, lemurs, macaques and others (Abdul-Latiff et al. 2014a;Mekonnen et al. 2018;Sgarlata et al. 2018;Kheng et al. 2018;Zinner et al. 2018;Liu et al. 2013;Wang et al. 2015;Abdul-Latiff et al. 2017). ...
The disjunct distribution of Presbytis femoralis subspecies across Sumatra (P. f. percura), southern (P. f. femoralis) and northern (P. f. robinsoni) Peninsular Malaysia marks the unique vicariance events in the Sunda Shelf. However, the taxonomic positions and evolutionary history of P. f. femoralis are unresolved after decades of research. To elucidate this evolutionary history, we analyzed 501 base pairs of the mitochondrial HVSI gene from 25 individuals representing Malaysia’s banded langur, with the addition of 29 sequences of Asian Presbytis from Genbank. Our results revealed closer affinity of P. f. femoralis to P. m. mitrata and P. m. sumatrana while maintaining the monophyletic state of P. f. femoralis as compared to P. f. robinsoni. Two central theses were inferred from the results; (1) P. f. femoralis does not belong in the same species classification as P. f. robinsoni, and (2) P. f. femoralis is the basal lineage of the Presbytis in Peninsular Malaysia. Proving the first hypothesis through genetic analysis, we reassigned P. f. femoralis of Malaysia to Presbytis neglectus (Schlegel’s banded langur) (Schlegel in Revue Methodique, Museum d'Histoire Naturelle des Pays-Bas 7:1, 1876) following the International Code of Zoological Nomenclature (article 23.3). The ancestors of P. neglectus are hypothesized to have reached southern Peninsular Malaysia during the Pleistocene and survived in refugium along the western coast. Consequently, they radiated upward, forming P. f. robinsoni and P. siamensis resulting in the highly allopatric distribution in Peninsular Malaysia. This study has successfully resolved the taxonomic position of P. neglectus in Peninsular Malaysia while providing an alternative biogeographic theory for the Asian Presbytis.
... In contrast, the CF habitat has areas with thick understory cover, where it was not always possible to sample only from identified individuals. Hence, we followed a particular group for up to one day and collected droppings within a short time interval whenever there was an opportunity [42,43]. Since we collected only a few samples from each groupmuch less than the actual group sizes [13]-the probability of sampling any one individual more than once was small. ...
Species with a restricted geographic distribution, and highly specialized habitat and dietary requirements, are particularly vulnerable to extinction. The Bale monkey (Chlorocebus djamdjamensis) is a little-known arboreal, bamboo-specialist primate endemic to the southern Ethiopian Highlands. While most Bale monkeys inhabit montane forests dominated by bamboo, some occupy forest fragments where bamboo is much less abundant. We used mitochondrial DNA (mtDNA) sequences to analyse the genetic structure and evolutionary history of Bale monkeys covering the majority of their remaining distribution range. We analysed 119 faecal samples from their two main habitats, continuous forest (CF) and fragmented forests (FF), and sequenced 735 bp of the hypervariable region I (HVI) of the control region. We added 12 orthologous sequences from congeneric vervets (C. pygerythrus) and grivets (C. aethiops) as well as animals identified as hybrids, previously collected in southern Ethiopia.
We found strong genetic differentiation (with no shared mtDNA haplotypes) between Bale monkey populations from CF and FF. Phylogenetic analyses revealed two distinct and highly diverged clades: a Bale monkey clade containing only Bale monkeys from CF and a green monkey clade where Bale monkeys from FF cluster with grivets and vervets. Analyses of demographic history revealed that Bale monkey populations (CF and FF) have had stable population sizes over an extended period, but have all recently experienced population declines.
The pronounced genetic structure and deep mtDNA divergence between Bale monkey populations inhabiting CF and FF are likely to be the results of hybridization and introgression of the FF population with parapatric Chlorocebus species, in contrast to the CF population, which was most likely not impacted by hybridization. Hybridization in the FF population was probably enhanced by an alteration of the bamboo forest habitat towards a more open woodland habitat, which enabled the parapatric Chlorocebus species to invade the Bale monkey's range and introgress the FF population. We therefore propose that the CF and FF Bale monkey populations should be managed as separate units when developing conservation strategies for this threatened species.
... The phylogenetic relationship revealed by mtDNA sequences shows that T. leucocephalus constitutes a monophyletic clade nested within the François' langur (Trachypithecus francoisi), from which it diverged 0.46-0.27 Myr ago (Liu et al., 2013). Thus, possible explanations for low genetic variation in the species may include its relatively short evolutionary history, restricted historical population size and recent population declines due to habitat deterioration and hunting by humans. ...
Habitat fragmentation may strongly impact population genetic structure and reduce the genetic diversity and viability of small and isolated populations. The white-headed langur (Trachypithecus leucocephalus) is a critically endangered primate species living in a highly fragmented and human-modified habitat in southern China. We examined the population genetic structure and genetic diversity of the species and investigated the environmental and anthropogenic factors that may have shaped its population structure. We used 214 unique multi-locus genotypes from 41 social groups across the main distribution area of T. leucocephalus, and found strong genetic structure and significant genetic differentiation among local populations. Our landscape genetic analyses using a causal modelling framework suggest that a large habitat gap and geographical distance represent the primary landscape elements shaping genetic structure, yet high levels of genetic differentiation also exist between patches separated by a small habitat gap or road. This is the first comprehensive study that has evaluated the population genetic structure and diversity of T. leucocephalus using nuclear markers. Our results indicate strong negative impacts of anthropogenic land modifications and habitat fragmentation on primate genetic connectivity between forest patches. Our analyses suggest that two management units of the species could be defined, and indicate that habitat continuity should be enforced and restored to reduce genetic isolation and enhance population viability.Heredity advance online publication, 15 February 2017; doi:10.1038/hdy.2017.2.
... Trachypithecus francoisi and T. leucocephalus 0.27-0.46 Liu et al. (2013) Trachypithecus francoisi and T. poliocephalus 0.25-0.50 Liu et al. (2013) Trachypithecus obscurus and T. phayrei 0.36 He et al. (2012) Trachypithecus cristatus and T. germaini 0.55 He et al. (2012) Rhinopithecus bieti and R. strykeri 0.24 Liedigk et al. (2012) 0.30 Zhou et al. (2014) Pygathrix cinerea and P. nemaeus 0.23 Liedigk et al. (2012) this specimen in fact originated in Myanmar, and was bought in Tengchong. ...
... Liu et al. (2013) Trachypithecus francoisi and T. poliocephalus 0.25-0.50 Liu et al. (2013) Trachypithecus obscurus and T. phayrei 0.36 He et al. (2012) Trachypithecus cristatus and T. germaini 0.55 He et al. (2012) Rhinopithecus bieti and R. strykeri 0.24 Liedigk et al. (2012) 0.30 Zhou et al. (2014) Pygathrix cinerea and P. nemaeus 0.23 Liedigk et al. (2012) this specimen in fact originated in Myanmar, and was bought in Tengchong. ...
We describe a species of Hoolock gibbon (Primates: Hylobatidae) that is new to science from eastern Myanmar and southwestern China. The genus of hoolock gibbons comprises two previously described living species, the western (Hoolock hoolock) and eastern hoolock (H. leuconedys) gibbons, geographically isolated by the Chindwin River. We assessed the morphological and genetic characteristics of wild animals and museum specimens, and conducted multi-disciplinary analyses using mitochondrial genomic sequences, external morphology, and craniodental characters to evaluate the taxonomic status of the hoolock population in China. The results suggest that hoolocks distributed to the east of the Irrawaddy-Nmai Hka Rivers, which were previously assigned to H. leuconedys, are morphologically and genetically distinct from those to the west of the river, and should be recognized as a new species, the Gaoligong hoolock gibbon or skywalker hoolock gibbon (H. tianxing sp. nov.). We consider that the new species should be categorized as Endangered under IUCN criteria. The discovery of the new species focuses attention on the need for improved conservation of small apes, many of which are in danger of extinction in southern China and Southeast Asia.
... With such dangerously low population numbers, historical hunting, and a disturbed, fragmented habitat, the Cat Ba langur is considered Critically Endangered ( Bleisch et al. 2008a) and has consistently been on the Top 25 Most Endangered Species List (2000)(2001)(2002)(2003)(2004)(2005)(2006)(2007)(2008)(2009)(2010)(2011)(2012)(2013)(2014)(2015)(2016) ( Leonard et al. 2016b). Despite this, however, there have been no long-term studies of this species; the only published papers/chapters on Cat Ba langurs focus on short-term, broad overviews ( Nadler and Ha Thang Long 2000;Schneider et al. 2010) and conservation options (Stenke and Chu Xuan Canh 2004; Schneider et al. 2010), with a few papers mentioning genetic work undertaken to define their taxonomy (Roos 2004; Liu et al. 2013a). Their long-term behavioural activity budget, how they move and use their habitat, social behaviour, and young development were completely undocumented before the start of this study. ...
... langurs independently diverged from François' langurs, achieving genetic separation by geographic barriers ( Liu et al. 2013a). As white-headed and François' langurs can hybridise ( Liu et al. 2013a), some suggest that white-headed langurs should be a subspecies of François' langurs ( Wang et al. 1997;Ding et al. 2000). ...
... langurs independently diverged from François' langurs, achieving genetic separation by geographic barriers ( Liu et al. 2013a). As white-headed and François' langurs can hybridise ( Liu et al. 2013a), some suggest that white-headed langurs should be a subspecies of François' langurs ( Wang et al. 1997;Ding et al. 2000). Regardless of species or subspecies status, both the Cat Ba and white-headed langurs are clearly part of the francoisi species-group ( Nadler et al. 2003;Roos 2004). ...
Cat Ba langurs (Trachypithecus poliocephalus), endemic to Cat Ba Island (Vietnam), are a member of the limestone langur group (francoisi species-group) found in Laos, Vietnam, and China. With less than 75 individuals in the world, these Cat Ba langurs are Critically Endangered. This dissertation represents the first long-term behavioural study of the species (549 contact hours across 11 months), and provides socioecological information for two groups (n=17-20) living on the Cua Dong fjord, which can be used in conservation management. Like most other colobines, the majority of the Cat Ba langur diet is leaves (84% of their dietary budget). This may explain their activity budget, which is primarily inactivity (55% of their activity budget), followed by foraging (19%) and social behaviour and locomotion (12% each). Activity and dietary budgets vary seasonally, with animals spending more time in social behaviours in the wet season, when they eat more fruit, and more time in foraging in the dry season, when leaves are ingested more, suggesting they are energy maximisers. In addition, age differences were found, with adults spending the most time in social behaviours and resting. Social behaviour primarily includes grooming and playing with others - play is more common in younger animals, while older animals tend to groom more. Overall, they spend 58% of their days not in proximity to any other langurs. Adult males spend the most time alone, and seem to avoid young langurs. Disputes tend to be between adult females, and two females only tend to come together if there is a young langur acting as a ‘social glue’. Home ranges varied between groups with the larger group’s range being 50ha compared to just 22ha for the smaller group. In both areas, rocks and sparsely covered areas are used most often, which is due to the shrubby, discontinuous vegetation. Most of the langurs’ observable time is spent on exposed slopes (47%), followed by steep cliffs (38%), summits (11%), valleys (3%), and the ground (1%); this varied seasonally, likely to balance foraging needs with thermoregulation. The langurs used 22 sleeping sites, including ledges (61%) and caves (17%). When newborn, Cat Ba langurs are bright orange. They start to lose this natal coat as an infant, and become much darker during the young juvenile stage. As individuals age, they also become more independent and start to forage and locomote more on their own. These reported behaviours can be used to create a baseline for activity budgets, home range size, and habitat use, and development and maturation that can be used for comparative purposes in future studies. Results find that animals are behaviourally similar to other related species and their biggest threat is likely their small, fragmented population structure. To combat this, I support habitat protection, patrols, and enforcement; education and training; habitat corridors; and limiting the human population, as these support an entire ecosystem while teaching locals the importance of biodiversity, reducing resource competition, and fragmentation from infrastructure, and providing a means for the langurs themselves to disperse.
... Moreover, non-invasive samples such as feces and hair usually yield low-quality DNA and working with mtDNA is easier and more reliable due to their availability in high copy number in cells. The hypervariable region has also been used to study the evolution of pelage coloration in colobine species [41]. ...
Gee's golden langur (Trachypithecus geei) is an endangered colobine primate, endemic to the semi-evergreen and mixed-deciduous forests of Indo-Bhutan border. During the last few decades, extensive fragmentation has caused severe population decline and local extinction of golden langur from several fragments. However, no studies are available on the impact of habitat fragmentation and the genetic diversity of golden langur in the fragmented habitats. The present study aimed to estimate the genetic diversity in the Indian population of golden langur. We sequenced and analyzed around 500 bases of the mitochondrial DNA (mtDNA) hypervariable region-I from 59 fecal samples of wild langur collected from nine forest fragments. Overall, genetic diversity was high (h = 0.934, π = 0.0244) and comparable with other colobines. Populations in smaller fragments showed lower nucleotide diversity compared to the larger forest fragments. The median-joining network of haplotypes revealed a genetic structure that corresponded with the geographical distribution. The Aie and Champabati Rivers were found to be a barrier to gene flow between golden langur populations. In addition, it also established that T. geei is monophyletic but revealed possible hybridization with capped langur, T. pileatus, in the wild. It is hoped that these findings would result in a more scientific approach towards managing the fragmented populations of this enigmatic species.
... With a total population of less than 1000 individuals living in the wild, it is listed as critically endangered in the IUCN Red List (Bleisch et al. 2008). Analysis of mitochondrial DNA sequences indicates low genetic diversity and strong geographical differentiation both among and within local populations (Liu et al. 2013b;Wang et al. 2015). However, essential population genetic parameters at the level of social units and individuals can only be inferred from nuclear DNA markers and remain unknown. ...
Genetic information can be critical in identifying conservation priorities and developing conservation strategies. There is an urgent need for noninvasive genetic tools to study the wild populations of Asian colobine monkeys. The majority of these species are threatened with habitat destruction, population reduction and even extinction, but generally lack information on their genetic diversity and population structure. Genetic sampling and tissue collection have been scarce in these species owing to strict regulations on manipulation of endangered species, and the difficulties and risks associated with capturing these arboreal and fast-moving monkeys in the challenging environments that they inhabit. These difficulties have hindered the development of molecular genetic markers, which are usually derived from tissues or blood. In this study, we present a method for de novo microsatellite isolation and genotyping using DNA from noninvasive origins of a critically endangered Asian colobine, the white-headed langur (Trachypithecus leucocephalus). Genomic DNA isolated from hair was shown to be sufficient for microsatellite enrichment and isolation, with similar isolation efficiencies as from tissue DNA. We identified and characterized 20 polymorphic microsatellite loci, and evaluated their amplification success and genotyping reliability with 86 field-collected fecal samples. The results show that this panel of loci can produce reliable genotypes from fecal samples, and represent a useful tool for noninvasive investigation of genetic structure, individual identification and kinship assessment in this highly endangered species. Our approach can be applied to conservation genetic studies of other wild species that lack sequence information and tissue samples. This article is protected by copyright. All rights reserved.
