Age‐specific effect of heterozygosity on survival in alpine marmots, Marmota marmota

Abstract

The fitness consequences of heterozygosity and the mechanisms underpinning them are still highly controversial. Using capture-mark-recapture models, we investigated the effects of individual heterozygosity, measured at 16 microsatellite markers, on age-dependent survival and access to dominance in a socially monogamous mammalian species, the alpine marmot. We found a positive correlation between standardized multilocus heterozygosity and juvenile survival. However, there was no correlation between standardized multilocus heterozygosity and either survival of older individuals or access to dominance. The disappearance of a significant heterozygosity fitness correlation when individuals older than juveniles are considered is consistent with the prediction that differences in survival among individuals are maximal early in life. The lack of a correlation between heterozygosity and access to dominance may be a consequence of few homozygous individuals attaining the age at which they might reach dominance. Two hypotheses have been proposed to explain heterozygosity-fitness correlations: genome-wide effects reflected by all markers or local effects of specific markers linked to genes that determine fitness. In accordance with genome-wide effects of heterozygosity, we found significant correlations between heterozygosities calculated across single locus or across two sets of eight loci. Thus, the genome-wide heterozygosity effect seems to explain the observed heterozygosity-fitness correlation in the alpine marmot.

Age‐dependent, negative heterozygosity–fitness correlations and local effects in an endangered Caribbean reptile, Iguana delicatissima

“…Assuming the hatchling cohort is representative of a proportion of the adult cohort and that the loci used in this study are representative of inbreeding levels within individuals, there is no evidence that selection against inbreeding shapes heterozygosity in the adults. Additionally, we predicted stronger positive correlations between heterozygosity and fitness in hatchlings than in adults due to selection against homozygous individuals (Cohas et al., 2009). Our data, however, demonstrate no significant positive HFCs in adults or hatchlings.…”

“…The population dynamics of aging cohorts may have a large effect on HFC detection if unfit genotypes are less common in the surviving individuals (David & Jarne, 1997), which may mask the true effects of inbreeding on fitness when only an older cohort is sampled. For example, Cohas, Bonenfant, Kempenaers, and Allainé (2009) detected inbreeding depression among juvenile alpine marmots, as multilocus heterozygosity (MLH) correlated strongly with juvenile survival. Among adult marmots, however, no correlation between MLH and fitness was revealed (Cohas et al., 2009).…”

“…For example, Cohas, Bonenfant, Kempenaers, and Allainé (2009) detected inbreeding depression among juvenile alpine marmots, as multilocus heterozygosity (MLH) correlated strongly with juvenile survival. Among adult marmots, however, no correlation between MLH and fitness was revealed (Cohas et al., 2009). Recent studies have further emphasized the importance of assessing multiple age classes in the detection and direction of HFCs (Annavi et al., 2014; Brommer et al., 2015; Canal et al., 2014; Monceau, Wattier, Dechaume‐Moncharmont, Dubreuil, & Cezilly, 2013).…”

Viability selection creates negative heterozygosity–fitness correlations in female Black Grouse Lyrurus tetrix

“…Similar to body size, the relationship between survival and heterozygosity has been mainly found in juveniles (e.g. Bean et al 2004;AcevedoWhitehouse et al 2006;Cohas et al 2009), but there is growing evidence that these effects continue throughout adulthood (Velando et al 2015;Cézilly et al 2016). We do not have data directly linking individual chick mortality and heterozygosity, but it is likely to be significant because of the strong relationship between inbreeding depression and chick mass (Soulsbury et al 2011), which in itself is a major determinant of chick survival (Ludwig et al 2010).…”

Large-scale genotyping of highly polymorphic loci by next-generation sequencing: how to overcome the challenges to reliably genotype individuals?

“…Concerning MHC class II loci, between 7 and 38 alleles were found in 10 rodent species (Goüy de Bellocq et al, 2008), and 60 and 61 in two loci in Gray mouse lemur (Microcebus murinus; Huchard et al, 2012). In addition to poor MHC diversity, low levels of genetic variability in Alpine marmots have been previously found using allozymes (Arnold, 1990;Preleuthner and Pinsker, 1993), minisatellites (Arnold, 1990;Rassmann et al, 1994;Kruckenhauser et al, 1997) and microsatellites (Cohas et al, 2009, but see Goossens et al, 2001) and this in different populations spread across the whole Alpine arc. Alpine marmots were widespread in Europe until the early Holocene (Couturier, 1955;Besson, 1971).…”