Vol.:(0123456789) 1 3
Primates
https://doi.org/10.1007/s10329-019-00750-z
ORIGINAL ARTICLE
Genetic differentiation and diversity of the Bolivian endemic titi
monkeys, Plecturocebus modestus and Plecturocebus olallae
Julia Barreta Pinto
1
· Jesús Martinez
2
· Yahaira Bernal
1
· Rolando Sánchez
1
· Robert Wallace
2
Received: 4 December 2018 / Accepted: 20 August 2019
© Japan Monkey Centre and Springer Japan KK, part of Springer Nature 2019
Abstract
The genetic variability of New World primates is still poorly documented. We present the first genetic study on two threat-
ened endemic titi monkey species in northern Bolivia (Plecturocebus modestus and Plecturocebus olallae) using six micro-
satellite markers to investigate genetic structure and variability of 54 individuals from two wild populations. A low level
of genetic diversity was found (34 alleles in the total sampled population). Locus 1118 presented the greatest number of
alleles. The mean number of alleles per locus in the total population was 5.6 and the average heterozygosity was 0.38 (range
0.12–0.88). The F
IS
value for the total population using all microsatellite loci shows a statistically significant heterozygote
deficit. The inbreeding coefficients (F
IS
) were positive and significantly different from zero (0.064 for P. olallae and 0.213
for P. modestus). The genetic differentiation between populations (F
ST
) was moderate with a pair-wise F
ST
estimate of 0.14.
Population structure analyses assigned the two populations to two differentiated clusters (K = 2). These results suggest that
these two species with very close distributional ranges arose from a single population, and that they remain in a process
of genetic differentiation and speciation. This study further underlines the urgent need for conservation actions for both
endemic primate species.
Keywords Olalla brothers monkey · Beni titi monkey · Microsatellites · Genetic diversity · Conservation
Introduction
The study of genetic variation and population structure is
critical to better understand how species evolve, adapt and
co-exist, as well as to propose rational conservation and
management strategies (Eguiarte 1990). Molecular markers
provide an estimate of genetic diversity, with multiple alleles
being useful in detecting heterozygosity and polymorphism
levels in natural populations, determining inter- and intra-
population relations, characterizing genetic population
structure, and analyzing genetic distances for evolutionary
studies (Avise 2000). As such, genetic studies are increas-
ingly relevant to taxonomy, biodiversity conservation and
environmental monitoring programs to ensure adequate
management of species and populations (Groom 2006).
The Olalla brothers’ titi monkey (Plecturocebus olallae)
and the Beni titi monkey (Plecturocebus modestus) are two
endemic primate species in Bolivia, which were described
by Lönnberg (1939). Although their type localities are less
than 65 km apart (Fig. 1), the respective specimens were
consistently considered as belonging to two different spe-
cies in a series of taxonomic assessments for the entire Cal-
licebinae group (Hershkovitz 1990; Kobayashi 1995; Van
Roosmalen et al. 2002; Wallace et al. 2013). Studies on
the distribution of both species have confirmed the pres-
ence of two similar, but phenotypically distinct forms that
correspond to the original descriptions with distributional
ranges quite close to each other (Fig. 1; Felton et al. 2006;
Martinez and Wallace 2007, 2013; Martínez and Wallace
2010; Martinez et al., 2013). The two Bolivian titi monkey
species were considered Endangered by the IUCN (Veiga
et al. 2008a, b), however in the most recent assessment P.
Electronic supplementary material The online version of this
article (https://doi.org/10.1007/s10329-019-00750-z) contains
supplementary material, which is available to authorized users.
* Julia Barreta Pinto
jbarretapinto@yahoo.com
1
Instituto de Biología Molecular y Biotecnología,
Universidad Mayor de San Andrés, UMSA, Cota Cota Calle
27 s/n, La Paz, Bolivia
2
Wildlife Conservation Society (WCS), Greater
Madidi-Tambopata Landscape Conservation Program, Casilla
3-35181, San Miguel, La Paz, Bolivia