Conservation implications of living in forest remnants: Inbreeding and genetic structure of the northernmost mantled howler monkeys

Abstract

The current unprecedented rates of environmental perturbation, particularly in rain forest ecosystems, are jeopardizing the persistence of a variety of tropical species.The development of adequate conservation programs requires incorporating the evolutionary history and population genetic information of species, especially in those threatened by habitat loss and fragmentation. Mexican mantled howler monkeys (Alouatta palliata mexicana) represent the northernmost distribution of primates in America, a Critically Endangered species mainly inhabiting forest remnants. We assessed historical and contemporary patterns of genetic variation in A. p. mexicana populations from five regions across its geographic distribution in Mexico. We employed non-invasive sampling techniques and evaluated microsatellite loci and mitochondrial cytochrome b sequences from 127 individuals from 15 wild and two semi-captive populations. Our data demonstrate negative genetic effects on A. p. mexicana as a result of isolation, fragmentation, and small effective population size.Results revealed two mitochondrial lineages and three genetically differentiated nuclear clusters, along with reduced nuclear genetic diversity, limited gene flow, and significant inbreeding, associated with concurrent processes of historical dispersion and contemporary landscape changes. Accordingly, we argue that A. palliata mexicana in Mexico is an independently evolving unit that meets the criteria for being assigned as an Evolutionarily Significant Unit, crucial for the preservation of the howler monkeys' phylogenetic and functional diversity. The three genetic clusters identified are essential for the maintenance of the adaptive diversity and long-term survival of this howler subspecies. Our genetic approach and conservation recommendations may be useful for other endangered primates inhabiting fragmented populations.

Co-structure analysis and genetic associations reveal insights into pinworms (Trypanoxyuris) and primates (Alouatta palliata) microevolutionary dynamics

“…We predicted higher differentiation in the parasites due to their dependent and more restricted migration. However, despite the presence of two genetic clusters (West and East) in both parasites and their host, genetic structure and genetic differentiation, contrary to our prediction, were stronger in the host than in both pinworms species, in agreement with limited dispersal in the primate as previously documented for this species [ 40 – 42 ]. Mazé-Guilmo et al [ 5 ] suggest that variables related to host dispersal could be poor predictors of genetic patterns in parasites, and that alternative factors like the host’s and the parasite’s biology are also key drivers of the codistribution of their genetic variation.…”

“…Comparatively, most of the southeastern haplotypes (Comalcalco and Pichucalco) are only found in that particular region. The history of dispersion of howler monkeys across southern Mexico helps explain this pattern, which followed a colonization process from south to north [ 57 ], thus the northernmost populations are the most recent [ 42 ]. During such range expansion events, parasites can either travel with their host into new locations or never reach the newly established populations because they were lost in the process or because the migrants did not carry the parasite with them.…”

“…For each individual host, we amplified a 964 pb fragment from the mitochondrial cytochrome b gene (cyt -b ) and genotyped nine microsatellite markers. Details about host DNA amplification and genotyping (cyt- b and microsatellites loci) procedures are found in Solórzano-García et al [ 42 ]. For parasite DNA, individual pinworms were digested overnight at 56 °C in a solution containing 10 mM Tris–HCl (pH 7.6), 20 mM NaCl, 100 mM EDTA (pH 8.0), 1% Sarkosyl, and 0.1 mg/ml proteinase K. DNA was extracted from the supernatant using the DNAzol ® reagent (Molecular Research Center, Cincinnati, OH) according to the manufacturer’s instructions.…”

Forest maturity has a stronger influence on the prevalence of spider monkeys than howler monkeys in an anthropogenically impacted rainforest landscape

“…The howler monkey F:I ratio we observed (Table 2) is similar to that of groups of howler monkeys considered as stable (Zucker and Clarke 2003), and higher than those reported for groups in fragments of Los Tuxtlas (Cristóbal-Azkarate et al 2005;Solórzano-García and Rodríguez-Luna 2010). This points towards the groups being stable at the time we sampled, but our results need to be considered in the context of recent reports that show negative genetic effects on A. palliata mexicana as a consequence of limited gene flow and inbreeding, likely due to isolation, fragmentation, and small population sizes in areas that include the Uxpanapa Valley (Solórzano-García et al 2021).…”

Expanded Distribution and Predicted Suitable Habitat for the Critically Endangered Yellow-tailed Woolly Monkey (Lagothrix flavicauda) in Peru

“…Such altered ranges may isolate populations, enhancing the likelihood of inbreeding depression or local extinction (Ewers and Didham 2005; Calkins et al . 2021; Solórzano-Garcia et al . 2021).…”