Inbreeding depression in ring-tailed lemurs (Lemur catta): genetic diversity predicts parasitism, immunocompetence, and survivorship

Abstract

The consequences of inbreeding have been well studied in a variety of taxa, revealing that inbreeding has major negative impacts in numerous species, both in captivity and in the wild; however, as trans-generational health data are difficult to obtain for long-lived, free-ranging species, similar analyses are generally lacking for nonhuman primates. Here, we examined the long-term effects of inbreeding on numerous health estimates in a captive colony of ring-tailed lemurs (Lemur catta), housed under semi-natural conditions. This vulnerable strepsirrhine primate is endemic to Madagascar, a threatened hotspot of biodiversity; consequently, this captive population represents an important surrogate. Despite significant attention to maintaining the genetic diversity of captive animals, breeding colonies invariably suffer from various degrees of inbreeding. We used neutral heterozygosity as an estimate of inbreeding and showed that our results reflect genome-wide inbreeding, rather than local genetic effects. In particular, we found that genetic diversity affects several fitness correlates, including the prevalence and burden of Cuterebra parasites and a third (N = 6) of the blood parameters analyzed, some of which reflect immunocompetence. As a final validation of inbreeding depression in this captive colony, we showed that, compared to outbred individuals, inbred lemurs were more likely to die earlier from diseases. Through these analyses, we highlight the importance of monitoring genetic variation in captive animals-a key objective for conservation geneticists-and provide insight into the potential negative consequences faced by small or isolated populations in the wild.

Smelling wrong: hormonal contraception in lemurs alters critical female odour cues

“…(e) Genetic analyses Our genetic variables were extracted from a multigenerational dataset involving 81 individuals genotyped at 11-14 microsatellite loci [26,27,30]. As previously described, we had estimated genetic diversity using individual genomewide heterozygosity (H O ) and had estimated kinship using female-female (FF) and female -male (FM) pairwise genetic distances (identity index [31]).…”

The genetic legacy of extirpation and re-colonization in Vancouver Island wolves

“…The observation of introgressed dog mtDNA into Vancouver Island wolves highlights the importance of maintaining population sizes that are sufficient to avoid Allee effects. In addition, small wild populations may suffer from inbreeding depression (Spielman et al 2004;Charpentier et al 2008). Accordingly, management objectives and actions that seek to reduce wolf populations may be in conflict with prudent conservation policies.…”

Condition, innate immunity and disease mortality of inbred crows

“…Empirical evidence for disease costs of inbreeding has been documented in captive settings (e.g. Spielman et al 2004;Hawley et al 2005;Ross-Gillespie et al 2007;Charpentier et al 2008;Ilmonen et al 2008) as well as in an array of free-living taxa, including California sea lions (Zalophus californianus; Acevedo- Whitehouse et al 2003), Mediterranean striped dolphins (Stenella coeruleoalba; Valsecchi et al 2004), Galapagos hawks (Buteo galapagoensis; Whiteman et al 2006), Soay sheep (Ovis aries; Coltman et al 1999), harbour seals (Phoca vitulina; Rijks et al 2008) and American crows (Corvus brachyrhynchos; Townsend et al 2009a). In some studies, however, the relationship between inbreeding and disease is unclear (e.g.…”

“…Previous field studies have explored links between inbreeding and components of the immune response (Reid et al 2007), inbreeding and disease (e.g. Acevedo-Whitehouse et al 2003;Charpentier et al 2008;Townsend et al 2009a), immune response, condition and parasite load (Moller & Haussy 2007;Parejo & Silva 2009), and population-level genetic diversity, immune response and ectoparasite abundance (Whiteman et al 2006). To date, however, no studies have explicitly examined the links between inbreeding, immune response, condition and disease mortality of individuals in a wild, free-living population.…”