Inbreeding depression in a critically endangered carnivore

Norén, Karin; Godoy, Erika; Dalén, Love; Meijer, Tomas; Angerbjörn, Anders

doi:10.1111/mec.13674

Cited by 40 publications

(77 citation statements)

References 51 publications

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“…This conservation paradigm, strictly related to the extinction vortex metaphor (5), is supported by empirical evidence (6)(7)(8), but it is challenged by studies showing that selection can be powerful also at small population sizes (9,10) and that survival and even demographic expansion can occur with almost no genomic variation (11). Interestingly, if extinction does not occur, drift in small isolated groups can produce, or contribute to, genetic and phenotypic divergence, possibly leading to speciation (12,13).…”

mentioning

confidence: 79%

Survival and divergence in a small group: The extraordinary genomic history of the endangered Apennine brown bear stragglers

Benazzo

Trucchi

Cahill

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

149

132

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Survival and divergence in a small group: the extraordinary genomic history of the endangered Apennine brown bear stragglers 2 AbstractAbout 100 km east of Rome, in the Central Apennine mountains, a critically endangered population of approximately fifty brown bears live in complete isolation. Mating outside this population is prevented by several hundred kilometers of bear-free territories. We exploited this natural experiment to better understand the gene and genomic consequences of surviving at extremely small population size. First, we found that brown bear populations in Europe lost connectivity since Neolithic times, when farming communities expanded and forest burning was used for land clearance. In Central Italy, this resulted in a 40-fold population decline. The overall genomic impact of this decline included the complete loss of variation in the mitochondrial genome and along long stretches of the nuclear genome. Several private and deleterious amino acid changes were fixed by random drift; predicted effects include energy deficit, muscle weakness, anomalies in cranial and skeletal development, and reduced aggressiveness. Despite this extreme loss of diversity, Apennine bear genomes show non-random peaks of high variation, possibly maintained by balancing selection, at genomic regions significantly enriched for genes associated with immune and olfactory systems. Challenging the paradigm of increased extinction risk in small populations, we suggest that random fixation of deleterious alleles a) can be an important driver of divergence in isolation, b) can be tolerated when balancing selection prevents random loss of variation at important genes and c) is followed by or results directly in favorable behavioral changes. SignificanceA small and relict population of brown bears lives in complete isolation in the Italian Apennine mountains, providing a unique opportunity to study the impact of drift and selection on the genomes of a large endangered mammal and to reconstruct the phenotypic consequences and the conservation implications of such evolutionary processes. The Apennine bear is highly inbred and harbors very low genomic variation. Several deleterious mutations have been accumulated by drift. We found evidence that this is a consequence of habitat fragmentation in the Neolithic, when human expansion and land clearance shrank its habitat, and that retention of variation at immune system and olfactory receptor genes, as well as changes in diet and behavior, prevented the extinction of the Apennine bear.

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mentioning

confidence: 79%

Survival and divergence in a small group: The extraordinary genomic history of the endangered Apennine brown bear stragglers

Benazzo

Trucchi

Cahill

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

149

132

View full text Add to dashboard Cite

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“…A recently published pedigree analysis revealed that the population is composed of five contributing founders, of which the historical level of inbreeding is unknown, and displays a minimum inbreeding level corresponding to half-sibling matings (average inbreeding coefficient, f = 0.125; Norén et al 2016). Furthermore, the same study documented a pronounced cost of inbreeding depression by means of a significant reduction in first-year survival and reproductive success in inbred foxes (Norén et al 2016).…”

Section: Introductionmentioning

confidence: 94%

“…When reproduction was confirmed, adults (if previously ear-tagged) were visually identified and pups as well as untagged adults were ear-tagged and ear tissue was collected for genetic analysis (Norén et al 2016). Based on a total of 63 individuals (n males = 29, n females = 34) visually and/or genetically verified to survive their first year (Norén et al 2016), we used a two-step procedure to determine matings. We first conducted genetic parentage testing between adults visually observed with pups at a den site.…”

Section: Study Population and Background Datamentioning

confidence: 99%

“…When pups and adults matched in allelic composition, no further analysis was undertaken. If there was a mismatch between pups and adults, or adults were not sampled, we conducted a parentage analysis between pups and all adults, present in the population at the time (Norén et al 2016). To assess individualand population-level inbreeding coefficients (f obs ), as well as relationship between all mated pairs, we used a genetically verified pedigree including 205 individuals (n males = 106, n females = 99; Norén et al 2016) in combination with maximum likelihood relatedness calculations implemented in the software ML Relate (Kalinowski et al 2006) and validated in the software COLONY (Jones and Wang 2010).…”

Section: Study Population and Background Datamentioning

confidence: 99%

“…To assess individualand population-level inbreeding coefficients (f obs ), as well as relationship between all mated pairs, we used a genetically verified pedigree including 205 individuals (n males = 106, n females = 99; Norén et al 2016) in combination with maximum likelihood relatedness calculations implemented in the software ML Relate (Kalinowski et al 2006) and validated in the software COLONY (Jones and Wang 2010). This was based on microsatellite data for eleven loci with a combined probability of identity (PI) < 10 −7 (detailed procedure described in Norén et al 2012Norén et al , 2016. All handling of animals followed the ASM guidelines and were approved by a Swedish ethical permit (A131-07).…”

Section: Study Population and Background Datamentioning

confidence: 99%

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Mating patterns in an inbred Arctic carnivore

2018

Self Cite

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Mating patterns are highly context-dependent and the outcome of selection pressures formed by ecological factors, inbreeding levels and access to available partners. In small and inbred populations, matings are limited by high kin encounter rates and access to mates. In this paper, we use background pedigree data to investigate mating patterns and inbreeding avoidance in an isolated and critically endangered Arctic fox (Vulpes lagopus) population. Empirical data showed avoidance of matings within natal family. Based on 35 documented matings, we only recorded two full-sibling matings and these occurred between individuals from different natal families. Matings between second-order relatives, however, occurred to the same extent as between unrelated individuals. To test how this influenced the population development of inbreeding (f), we simulated scenarios of random mating, exclusion of natal family and exclusion of individuals in already existing pair bonds. The observed development of inbreeding did not correspond the expected scenario of random mating (linear regression, r 2 = 0.354, P = 0.20), but showed a comparable outcome as the simulated development of discriminating natal family (linear regression, r 2 = 0.980, P < 0.001). We conclude that behavioural, pre-copulatory inbreeding avoidance strategies occur in this population and that exclusion of mating with natal family causes a slower increase in inbreeding levels compared to random mating. This study demonstrates how long-term monitoring, pedigree construction and simulations can generate information valuable for an in-depth understanding of both conservation genetics and behavioural ecology in threatened populations.

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Small fish, large river: Surprisingly minimal genetic structure in a dispersal‐limited, habitat specialist fish

Washburn

Cashner

Blanton

2020

Ecology and Evolution

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Genetic connectivity is expected to be lower in species with limited dispersal ability and a high degree of habitat specialization (intrinsic factors). Also, gene flow is predicted to be limited by habitat conditions such as physical barriers and geographic distance (extrinsic factors). We investigated the effects of distance, intervening pools, and rapids on gene flow in a species, the Tuxedo Darter (Etheostoma lemniscatum), a habitat specialist that is presumed to be dispersal‐limited. We predicted that the interplay between these intrinsic and extrinsic factors would limit dispersal and lead to genetic structure even at the small spatial scale of the species range (a 38.6 km river reach). The simple linear distribution of E. lemniscatum allowed for an ideal test of how these factors acted on gene flow and allowed us to test expectations (e.g., isolation‐by‐distance) of linearly distributed species. Using 20 microsatellites from 163 individuals collected from 18 habitat patches, we observed low levels of genetic structure that were related to geographic distance and rapids, though these factors were not barriers to gene flow. Pools separating habitat patches did not contribute to any observed genetic structure. Overall, E. lemniscatum maintains gene flow across its range and is comprised of a single population. Due to the linear distribution of the species, a stepping‐stone model of dispersal best explains the maintenance of gene flow across its small range. In general, our observation of higher‐than‐expected connectivity likely stems from an adaptation to disperse due to temporally unstable and patchy habitat.

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Inbreeding depression in a critically endangered carnivore

Cited by 40 publications

References 51 publications

Survival and divergence in a small group: The extraordinary genomic history of the endangered Apennine brown bear stragglers

Survival and divergence in a small group: The extraordinary genomic history of the endangered Apennine brown bear stragglers

Mating patterns in an inbred Arctic carnivore

Small fish, large river: Surprisingly minimal genetic structure in a dispersal‐limited, habitat specialist fish

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