Genetic structure in the southernmost populations of black-and-gold howler monkeys (Alouatta caraya) and its conservation implications

Abstract

Black-and-gold howler monkeys Alouatta caraya, are arboreal primates, inhabitants of Neotropical forests, highly susceptible to the yellow fever virus, considered early 'sentinels' of outbreaks, and thus, of major epidemiological importance. Currently, anthropogenic habitat loss and modifications threatens their survival. Habitat modification can prevent, reduce or change dispersal behavior, which, in turn, may influence patterns of gene flow. We explored past and contemporary levels of genetic diversity, elucidated genetic structure and identified its possible drivers, in ten populations (n = 138) located in the southernmost distribution range of the species in South America, in Argentina and Paraguay. Overall, genetic variability was moderate (ten microsatellites: 3.16 ± 0.18 alleles per locus, allelic richness of 2.93 ± 0.81, 0.443±0.025 unbiased expected heterozygosity; 22 haplotypes of 491-bp mitochondrial Control Region, haplotypic diversity of 0.930 ± 0.11, and nucleotide diversity of0.01± 0.007). Significant evidence of inbreeding was found in a population that was, later, decimated by yellow fever. Population-based gene flow measures (FST = 0.13; θST = 018), hierarchical analysis of molecular variance and Bayesian clustering methods revealed significant genetic structure, grouping individuals into four clusters. Shared haplotypes and lack of mitochondrial differentiation (non-significant θST) among some populations seem to support the hypothesis of historical dispersal via riparian forests. Current resistance analyses revealed a significant role of landscape features in modeling contemporary gene flow: continuous forest and riparian forests could promote genetic exchange, whereas disturbed forests or crop/grassland fields may restrict it. Estimates of effective population size allow anticipating that the studied populations will lose 75% of heterozygosity in less than 50 generations. Our findings suggest that anthropogenic modifications on native forests, increasingly ongoing in Northeastern Argentina, Southern Paraguay and Southeastern Brazil, might prevent the dispersal of howlers, leading to population isolation. To ensure long-term viability and maintain genetic connectivity of A. caraya remnant populations, we recommend preserving and restoring habitat continuity. To conserve the species genetic pool, as well, the four genetic clusters identified here should be considered separate Management Units and given high conservation priority. In light of our findings and considering complementary non-genetic information, we suggest upgrading the international conservation status of A. caraya to “Vulnerable”.

Reduced geographic variation in roars in different habitats rejects the acoustic adaptation hypothesis in the black‐and‐gold howler monkey (Alouatta caraya)

“…This is the only site where howler monkey roars need to travel through open grasslands to reach groups inhabiting other forest patches, 2—Parque Nacional Chaco (PN Chaco, 26°48′S; 59°36′W), a riverine forest along the Negro River, 3—Reserva privada Guaycolec (Guaycolec 25°54′S; 58°13′W), a tall and dense riverine forest along the Pilagá River, and 4—Reserva de Vida Silvestre Yacutinga (Yacutinga 25°35′S; 54°03′W), a typical dense and closed subtropical forest. The genetic structure of the four A. caraya study populations demonstrated three genetically differentiated clusters: (K1) EBCo, (K2) PN Chaco and Guaycolec, and (K3) Yacutinga (Oklander et al, ; Figure b).…”

“…Sampled populations are separated with white dashed lines. Equally color populations share genetic ancestry (modified from Oklander et al ) [Colour figure can be viewed at wileyonlinelibrary.com]…”

“…We worked at four sites with naturally occurring populations of A. Yacutinga (Oklander et al, 2017; Figure 1b).…”

“…The black‐and‐gold howler monkey ( Alouatta caraya ) occupies a wide geographic range in South America and occupies structurally different habitats that may impose distinctive challenges for communication over long distances, including closed subtropical moist forests, dry forests, and semi‐open forest patches surrounded by grasslands (Holzmann et al, ). No subspecies have been recognized on morphological and genetic grounds (Cortés‐Ortiz, Rylands, & Mittermeier, ), although population genetic studies show the existence of geographic structuring in clusters based on nuclear genetic diversity (Oklander, Miño, Fernández, Caputo, & Corach, ). Vocalizations in howlers are thought to be genetically determined, and to this day, there is no definitive evidence of vocal learning in non‐human primates (reviewed in Egnor & Hauser, ; but see Ghazanfar, Liao, & Takahashi, ).…”

“…Sampled populations are separated with white dashed lines. Equally color populations share genetic ancestry (modified from Oklander et al 2017) [Colour figure can be viewed at wileyonlinelibrary.com] 2010; rails: Rek & Kwiatkowska, 2016 and torrent frogs: Goutte et al, 2018). Evidence gathered over the years provided partial support to this theoretical framework (reviewed in Ey & Fisher, 2009), in part because other factors beyond vegetation type and/or environmental sound come into play influencing vocalization structure.…”