Genetic Consequences of Habitat Fragmentation in Black-and-Gold Howler (Alouatta caraya) Populations from Northern Argentina

Abstract

Human-induced habitat fragmentation might seriously affect behavioural patterns and the survival of species whose ecological requirements strongly depend on specific environmental conditions. We compared the genetic structure and dispersal patterns of 2 populations of Alouatta caraya (Plathyrrhini, Atelidae) to understand how habitat reduction and fragmentation affect gene flow in this species. We sampled individuals from 7 groups living in continuous forest (CF, n=46, 22 males and 24 females), and 11 groups that inhabit a fragmented forest (FF, n=50, 24 males and 26 females). FST values based on 11 microsatellite loci showed a recent genetic differentiation among groups in the FF. In contrast, the CF showed no differentiation among groups. Further, FST values between sexes, as well as kinship relationships, also exhibited differences between habitats. In the CF, both males and females disperse, leading to nondifferentiated groups composed of adults that are not close relatives. Conversely, in the FF, some groups are differentiated, males disperse more than females, and groups are composed of closely related adult females. Our results suggest that habitat fragmentation modifies the dispersal patterns of black-and-gold howlers. These differences between habitats may reflect a reduced gene flow, providing genetic evidence that suggests that habitat fragmentation severely limits the howler's ability to disperse. An increasing level of isolation due to uncontrolled deforestation may cause similar loss of genetic diversity on other arboreal primates, and nonprimates that depend on Int J Primatol (2010) 31:813-832

Kin structure and parallel dispersal in the black-and-gold howler monkey Alouatta caraya (Platyrrhini, Atelidae)

“…In A. pigra, which is also characterized by bisexual dispersal, females may disperse when group size increases and initiate a new group or join another smaller group (Ostro et al, 2001), possibly due to a decrease in reproductive success (Treves, 2001;Van Belle and Estrada, 2008). Oklander et al (2010) observed different patterns of dispersal in A. caraya groups from continuous and fragmented forests, revealing male-biased dispersal in fragmented habitats. In the present study, we found that female Alc29 (Figure 3) from social group 5 was identified as the candidate mother of five siblings, and four of these were the product of extra-group copulations.…”

“…We hypothesize that the lack of suitable habitat may decrease opportunities for dispersal and the formation of new groups, causing a biased sex ratio and mating pattern. In fact, we detected many cases of extra-group copulations (see Figure 3), which may indicate a rupture in social group structure due to a reduction in habitat quality (Zunino et al, 2001Oklander et al, 2010). A. caraya living in fragmented forests in Argentina tend to be one male groups, whereas those in more productive and continuous forests are multi-male groups (Kowalewski and Garber, 2010).…”

“…For instance, populations of A. pigra from Belize presented lower heterozygosity (0.43; Winkler et al, 2004). Alouatta seniculus from Colombia also have a relatively low value of genetic diversity (0.469; Ruiz-Garcia et al, 2007a), as do populations of A. caraya from North Argentina (~0.50; Oklander et al, 2010). Nevertheless, four species from Central and South America, A. seniculus, A. macconnelli, A. caraya, and A. palliata, presented higher values (average ~0.70, Ruiz-Garcia et al, 2007b) than were found in the present study.…”

“…Male-biased dispersal has been reported in some Atelidae genera, such as Brachyteles, Ateles, and Lagothrix (Di Fiore and Fleischer, 2005) based on behavioral observations, with bisexual dispersal reported in Alouatta (Strier, 2011). Oklander et al (2010) observed different patterns of dispersal in black-and-gold howler monkey (Alouatta caraya) groups from continuous and fragmented forests. In Alouatta pigra, females may disperse when the social group increases in size and initiate a new group or join another group (Ostro et al, 2001).…”

“…Ecological studies and behavioral observations have shown that dispersal is either not sexbiased (Rumiz, 1990;Calegaro-Marques and Bicca-Marques, 1996) or may vary depending on habitat quality. For instance, habitat fragmentation may modify dispersal patterns, increasing male-biased dispersal, or limiting the ability for males and females to disperse, thereby reducing gene flow (Oklander et al, 2010).…”