Phylogeographic evidence for two species of muriqui (genus Brachyteles)

Abstract

The taxonomy of muriquis, the largest extant primates in the New World, is controversial. While some specialists argue for a monotypic genus (Brachyteles arachnoides), others favor a two-species classification, splitting northern muriquis (Brachyteles hypoxanthus) from southern muriquis (B. arachnoides). This uncertainty affects how we study the differences between these highly endangered and charismatic primates, as well as the design of more effective conservation programs.To address this issue, between 2003 and 2017 we collected over 230 muriqui fecal samples across the genus' distribution in the Brazilian Atlantic Forest, extracted DNA from these samples, and sequenced 423 base pairs of the mitochondrial DNA (mtDNA) control region. Phylogenetic and species delimitation analyses of our sequence dataset robustly support two reciprocally monophyletic groups corresponding to northern and southern muriquis separated by an average 12.7% genetic distance. The phylogeographic break between these lineages seems to be associated with the Paraíba do Sul River and coincides with the transition between the north and south Atlantic Forest biogeographic zones. Published divergence estimates from whole mitochondrial genomes and nuclear loci date the split between northern and southern muriquis to the Early Pleistocene (ca. 2.0 mya), and our new mtDNA dataset places the coalescence time for each of these two clades near the last interglacial (ca. 120-80 kya). Our results, together with both phenotypic and ecological differences, support recognizing northern and southern muriquis as sister species that should be managed as distinct evolutionarily significant units. Given that only a few thousand muriquis remain in nature, it is imperative that conservation strategies are tailored to protect both species from extinction.

Phylogeography, genetic diversity, and intraspecific genetic structure of the black‐horned capuchin (Sapajus nigritus)

“…species of muriquis, Brachyteles hypoxanthus and B. arachnoides that diverged about 2 Ma(Chaves et al, 2019). The Paraíba do Sul River probably also drove the strong phylogenetic break observed between the northern clade and southern clade of S. nigritus analyzed here.Within the southern clade, the diversification between populationsNorth and South of the Tietê River suggests that this river might had affected the gene flow in this region.…”

The limits of resilience

“…Muriquis are the largest nonhuman primates of the Americas, and endemic to the Atlantic Forest of southeastern Brazil. The northern muriqui was previously classified with the southern muriqui in a monotypic genus, Brachyteles arachnoides, but taxonomic revisions based on morphological and molecular analyses have led to its reclassification as a distinct species, B. hypoxanthus, with the divergence from the southern muriqui estimated to have occurred about 2 million years ago (reviewed by Chaves et al 2019). Similar to the plights of many other threatened primates in the Brazilian Atlantic Forest and throughout the tropics, past and ongoing habitat destruction and hunting pressures have fragmented their populations and reduced their total numbers.…”

Science, Policy, and Conservation Management for a Critically Endangered Primate in the Atlantic Forest of Brazil

“…It was not until the early 1980s, however, that the first long-term studies were launched. At that time the muriqui was classified as a monotypic species, Brachyteles arachnoides, and it was not until the early 2000s that the separation of the genus into two species was widely recognized, with molecular data marking their split at c. 2 million years (reviewed by Chaves et al, 2019). The reclassification of the northern muriqui from B. arachnoides to B. hypoxanthus makes prior literature confusing to non-experts, who may not appreciate that the northern muriqui had been studied for decades before it was given its own species name (Strier, 2018).…”

“…For example, the workshops that generated the PAN Muriquis were directly responsible for the development of criteria for prioritizing muriqui populations regarding their demographic, genetic, and geographic importance for the species' conservation (Strier et al, 2017). They also facilitated the data sharing that enabled comparative analyses of natural demographic fluctuations (Strier et al, 2019), the impact of management and natural dispersal processes on population size and composition (Tabacow et al, 2021), the genetics that demonstrate the 2 MY split, and insights into population histories that distinguish the northern and southern species (Chaves et al, 2019). The objectives of the PAN Muriquis also called for coordinated assessments and reassessments of the status of all populations of muriquis, to which the most up-to-date technologies, such as arboreal cameras and drones with infrared cameras, have been applied (Melo, 2021;Tabacow et al, in press, a).…”