Ancient divergence of Indian and Tibetan wolves revealed by recombination-aware phylogenomics.

The grey wolf (Canis lupus) expanded its range across Holarctic regions during the late Pleistocene. Consequently, most grey wolves share recent (<100,000 years ago) maternal origins corresponding to a widespread Holarctic clade. However, two deeply divergent (200,000-700,000 years ago) mitochondrial clades are restricted, respectively, to the Indian subcontinent and the Tibetan Plateau, where remaining wolves are endangered. No genome-wide analysis had previously included wolves corresponding to the mitochondrial Indian clade or attempted to parse gene flow and phylogeny. We sequenced four Indian and two Tibetan wolves and included 31 additional canid genomes to resolve the phylogenomic history of grey wolves. Genomic analyses revealed Indian and Tibetan wolves to be distinct from each other and from broadly distributed wolf populations corresponding to the mitochondrial Holarctic clade. Despite gene flow, which was reflected disproportionately in high-recombination regions of the genome, analyses revealed Indian and Tibetan wolves to be basal to Holarctic grey wolves, in agreement with the mitochondrial phylogeny. In contrast to mitochondrial DNA, however, genomic findings suggest the possibility that the Indian wolf could be basal to the Tibetan wolf, a discordance potentially reflecting selection on the mitochondrial genome. Together, these findings imply that southern regions of Asia have been important centers for grey wolf evolution and that Indian and Tibetan wolves represent evolutionary significant units (ESUs). Further study is needed to assess whether these ESUs warrant recognition as distinct species. This question is especially urgent regarding the Indian wolf, which represents one of the world's most endangered wolf populations.

Population genetic structure and evolutionary history of Bale monkeys (Chlorocebus djamdjamensis) in the southern Ethiopian Highlands.

BACKGROUND: 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. RESULTS: 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. CONCLUSIONS: 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.

Dietary flexibility of Bale monkeys (Chlorocebus djamdjamensis) in southern Ethiopia: effects of habitat degradation and life in fragments.

BACKGROUND: Understanding the effects of habitat modification on the feeding strategies of threatened species is essential to designing effective conservation management plans. Bale monkeys (Chlorocebus djamdjamensis) are endemic to the rapidly shrinking montane forests of the southern Ethiopian Highlands. Most populations inhabit continuous bamboo forest subsisting largely on the young leaves and shoots of a single species of bamboo. Because of habitat disturbance in recent decades, however, there are now also several dozen small populations inhabiting isolated forest fragments where bamboo has been degraded. During 12-months, we assessed Bale monkey responses to habitat degradation by comparing habitat composition, phenological patterns, and feeding ecology in a largely undisturbed continuous forest (Continuous groups A and B) and in two fragments (Patchy and Hilltop groups). RESULTS: We found that habitat quality and food availability were much lower in fragments than in continuous forest. In response to the relative scarcity of bamboo in fragments, Bale monkeys spent significantly less time feeding on the young leaves and shoots of bamboo and significantly more time feeding on non-bamboo young leaves, fruits, seeds, stems, petioles, and insects in fragments than in continuous forest. Groups in fragments also broadened their diets to incorporate many more plant species (Patchy: ≥ 47 and Hilltop: ≥ 35 species)-including several forbs, graminoids and cultivated crops-than groups in continuous forest (Continuous A: 12 and Continuous B: 8 species). Nevertheless, bamboo was still the top food species for Patchy group (30% of diet) as well as for both continuous forest groups (mean = 81%). However, in Hilltop group, for which bamboo was especially scarce, Bothriochloa radicans (Poaceae), a grass, was the top dietary species (15% of diet) and bamboo ranked 10th (2%). CONCLUSIONS: We demonstrate that Bale monkeys are more dietarily flexible than previously thought and able to cope with some degradation of their primary bamboo forest habitat. However, crop raiding and other terrestrial foraging habits more common among fragment groups may place them at greater risk of hunting by humans. Thus, longitudinal monitoring is necessary to evaluate the long-term viability of Bale monkey populations in fragmented habitats.

Flexibility in positional behavior, strata use, and substrate utilization among Bale monkeys (Chlorocebus djamdjamensis) in response to habitat fragmentation and degradation.

Studies of the effects of habitat fragmentation and degradation on primate positional behavior, strata use, and substrate utilization offer valuable insights into the behavioral and ecological flexibility of primates whose habitats have undergone extensive anthropogenic disturbance. In this study, we evaluated how positional behavior, strata use, and substrate utilization differed between Bale monkeys (Chlorocebus djamdjamensis)-bamboo-eating cercopithecids endemic to the southern Ethiopian Highlands-occupying continuous versus fragmented forests. Bale monkeys in forest fragments (where bamboo had been degraded or eradicated) spent significantly more time on the ground and in understory strata whereas those in continuous forest spent significantly more time in the middle and upper strata. Bale monkeys in forest fragments also spent significantly more time walking and galloping and significantly less time climbing than those in continuous forest. Our results suggest that, unlike the primarily arboreal Bale monkeys in continuous forest, Bale monkeys in forest fragments should be characterized as semi-terrestrial. In response to habitat disturbance in fragments, we observed a greater emphasis on terrestrial foraging and travel among Bale monkeys in these human altered habitats, which may put them at greater risk of predation and conflict with nearby human populations. Bale monkeys in fragments exhibit flexibility in their positional behavioral repertoire and their degree of terrestriality is more similar to their sister taxa in Chlorocebus than to Bale monkeys in continuous forest. These findings suggest that habitat alteration may compel Bale monkeys to exhibit semi-terrestrial behaviors crucial for their persistence in human-modified habitats. Our results contribute to a growing body of literature on primate behavioral responses to anthropogenic modification of their habitats and provide information that can contribute to the design of appropriate conservation management plans.

Impacts of habitat loss and fragmentation on the activity budget, ranging ecology and habitat use of Bale monkeys (Chlorocebus djamdjamensis) in the southern Ethiopian Highlands.

Understanding the extent to which primates in forest fragments can adjust behaviorally and ecologically to changes caused by deforestation is essential to designing conservation management plans. During a 12-month period, we studied the effects of habitat loss and degradation on the Ethiopian endemic, bamboo specialist, Bale monkey (Chlorocebus djamdjamensis) by comparing its habitat quality, activity budget, ranging ecology and habitat use in continuous forest and two fragments. We found that habitat loss and fragmentation resulted in major differences in vegetation composition and structure between forest types. We also found that Bale monkeys in continuous forest spent more time feeding and traveling and less time resting and socializing than monkeys in fragments. Bale monkeys in continuous forest also had higher movement rates (m/hr) than monkeys in fragments. Bale monkeys in continuous forest used exclusively bamboo and mixed bamboo forest habitats while conspecifics in fragments used a greater variety of habitats including human use areas (i.e., matrix). Our findings suggest that Bale monkeys in fragments use an energy minimization strategy to cope with the lower availability of the species' primary food species, bamboo (Arundinaria alpina). We contend that Bale monkeys may retain some of the ancestral ecological flexibility assumed to be characteristic of the genus Chlorocebus, within which all extant species except Bale monkeys are regarded as ecological generalists. Our results suggest that, like other bamboo eating primates (e.g., the bamboo lemurs of Madagascar), Bale monkeys can cope with a certain threshold of habitat destruction. However, the long-term conservation prospects for Bale monkeys in fragments remain unclear and will require further monitoring to be properly evaluated.

Ecological plasticity in the gastrointestinal microbiomes of Ethiopian Chlorocebus monkeys.

Human activities can cause habitat degradation that may alter the types and quality of available food resources and thus influence the microbiomes of wild animal populations. Furthermore, seasonal shifts in food availability may cause adaptive responses in the gut microbiome to meet the need for different metabolic capabilities. Here, we demonstrate local-scale population structure in the gastrointestinal microbiotas of Chlorocebus monkeys, in southern Ethiopia, in response to varying degrees of human encroachment. We further provide evidence of adaptation to ecological conditions associated with the dry and wet seasons, and show seasonal effects to be more pronounced in areas with limited human activity. Finally, we report species-level microbiota differences between the endemic Ethiopian Bale monkey, an ecological specialist, and generalist Chlorocebus species from the same geographical region.

Multilevel social structure and diet shape the gut microbiota of the gelada monkey, the only grazing primate.

BACKGROUND: The gelada monkey (Theropithecus gelada), endemic to the Ethiopian highlands, is the only graminivorous primate, i.e., it feeds mainly on grasses and sedges. In spite of known dental, manual, and locomotor adaptations, the intestinal anatomy of geladas is similar to that of other primates. We currently lack a clear understanding of the adaptations in digestive physiology necessary for this species to subsist on a graminoid-based diet, but digestion in other graminivores, such as ruminants, relies heavily on the microbial community residing in the gastrointestinal (GI) system. Furthermore, geladas form complex, multilevel societies, making them a suitable system for investigating links between sociality and the GI microbiota. RESULTS: Here, we explore the gastrointestinal microbiota of gelada monkeys inhabiting an intact ecosystem and document how factors like multilevel social structure and seasonal changes in diet shape the GI microbiota. We compare the gelada GI microbiota to those of other primate species, reporting a gradient from geladas to herbivorous specialist monkeys to dietary generalist monkeys and lastly humans, the ultimate ecological generalists. We also compare the microbiotas of the gelada GI tract and the sheep rumen, finding that geladas are highly enriched for cellulolytic bacteria associated with ruminant digestion, relative to other primates. CONCLUSIONS: This study represents the first analysis of the gelada GI microbiota, providing insights into the adaptations underlying graminivory in a primate. Our results also highlight the role of social organization in structuring the GI microbiota within a society of wild animals.

Large-scale genetic structuring of a widely distributed carnivore--the Eurasian lynx (Lynx lynx).

Over the last decades the phylogeography and genetic structure of a multitude of species inhabiting Europe and North America have been described. The flora and fauna of the vast landmasses of north-eastern Eurasia are still largely unexplored in this respect. The Eurasian lynx is a large felid that is relatively abundant over much of the Russian sub-continent and the adjoining countries. Analyzing 148 museum specimens collected throughout its range over the last 150 years we have described the large-scale genetic structuring in this highly mobile species. We have investigated the spatial genetic patterns using mitochondrial DNA sequences (D-loop and cytochrome b) and 11 microsatellite loci, and describe three phylogenetic clades and a clear structuring along an east-west gradient. The most likely scenario is that the contemporary Eurasian lynx populations originated in central Asia and that parts of Europe were inhabited by lynx during the Pleistocene. After the Last Glacial Maximum (LGM) range expansions lead to colonization of north-western Siberia and Scandinavia from the Caucasus and north-eastern Siberia from a refugium further east. No evidence of a Berinigan refugium could be detected in our data. We observed restricted gene flow and suggest that future studies of the Eurasian lynx explore to what extent the contemporary population structure may be explained by ecological variables.