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

Abstract

BackgroundSpecies 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.ResultsWe 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.ConclusionsThe 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.Electronic supplementary materialThe online version of this article (10.1186/s12862-018-1217-y) contains supplementary material, which is available to authorized users.

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

“…for example, C. pygerythrus 20% (Rose, ) and some Cercopithecus spp. [e.g., C. neglectus 30% (Gautier‐Hion, ), C. solatus 33.7% (Motsch et al, ), C. campbelli 20% (McGraw, ) and C. lhoesti 38% (Struhsaker, )] rather than the arboreal category that best fits the source populations of Bale monkeys in continuous forest (Mekonnen et al, in press).…”

Population Differentiation and Demographic History of the Cycas taiwaniana Complex (Cycadaceae) Endemic to South China as Indicated by DNA Sequences and Microsatellite Markers

“…AMOVA was conducted in Arlequin, version 3.0 (Excoffier et al, 2005) according to different species and distribution regions. To test for the correlation between genetic distance and geographic distance, the isolated by distance (IBD) model implemented in a mental test (Mantel, 1967) was performed in GenALEx, version 6.3. Genetic distance was calculated with Genepop, version 4.1.4 (Rousset, 2008) according to the formula F ST /(1 − F ST ).…”

“…Most tropical species experienced a relatively moderate temperature in the Pleistocene. However, climatic oscillations have also significantly affected the genetic structure, population dynamics, and divergence of many extant global flora and fauna (Pauls et al, 2013;Yang et al, 2016;Mekonnen et al, 2018). Historical processes (e.g., the Ice Age) have left marked imprints on the genetic structure of extant species, especially for long-evolved organisms (Lo´pez-Pujol et al, 2011;Liu et al, 2015).…”

A standardized approach to empirically define reliable assignment thresholds and appropriate management categories in deeply introgressed populations

“…Nevertheless, the detection of hybrids and backcrosses ( Supplementary Table S1a) can be further complicated by a number of technical or statistical issues. Many hybridizing taxa are elusive and difficult to detect, therefore hybridization monitoring programs are usually carried out relying on opportunistically-collected and often degraded biological materials 23,[29][30][31][32][33][34][35][36][37] . These approaches limit the use of more diagnostic large panels of markers such as Single Nucleotide Polymorphisms (SNPs) and the employment of more than a few tens of microsatellites (or STRs, Short Tandem Repeats), which generally allow the detection of hybridization events occurred only up to two or three generations in the past 5,38,39 .…”