Inbreeding (mating between relatives) is a major concern for conservation as it decreases individual fitness and can increase the risk of population extinction. We used whole-genome resequencing of 97 grey wolves (Canis lupus) from the highly inbred Scandinavian wolf population to identify 'identical-by-descent' (IBD) chromosome segments as runs of homozygosity (ROH). This gave the high resolution required to precisely measure realized inbreeding as the IBD fraction of the genome in ROH (F ). We found a striking pattern of complete or near-complete homozygosity of entire chromosomes in many individuals. The majority of individual inbreeding was due to long IBD segments (>5 cM) originating from ancestors ≤10 generations ago, with 10 genomic regions showing very few ROH and forming candidate regions for containing loci contributing strongly to inbreeding depression. Inbreeding estimated with an extensive pedigree (F ) was strongly correlated with realized inbreeding measured with the entire genome (r = 0.86). However, inbreeding measured with the whole genome was more strongly correlated with multi-locus heterozygosity estimated with as few as 500 single nucleotide polymorphisms, and with F estimated with as few as 10,000 single nucleotide polymorphisms, than with F. These results document in fine detail the genomic consequences of intensive inbreeding in a population of conservation concern.
Describing the evolutionary dynamics of now extinct populations is challenging, as their genetic composition before extinction is generally unknown. The Glanville fritillary butterfly has a large extant metapopulation in the Åland Islands in Finland, but declined to extinction in the nearby fragmented southwestern (SW) Finnish archipelago in the 20th century. We genotyped museum samples for 222 SNPs across the genome, including SNPs from candidate genes and neutral regions. SW Finnish populations had significantly reduced genetic diversity before extinction, and their allele frequencies gradually diverged from those in contemporary Åland populations over 80 y. We identified 15 outlier loci among candidate SNPs, mostly related to flight, in which allele frequencies have changed more than the neutral expectation. At outlier loci, allele frequencies in SW Finland shifted in the same direction as newly established populations deviated from old local populations in contemporary Åland. Moreover, outlier allele frequencies in SW Finland resemble those in fragmented landscapes as opposed to continuous landscapes in the Baltic region. These results indicate selection for genotypes associated with good colonization capacity in the highly fragmented landscape before the extinction of the populations. Evolutionary response to habitat fragmentation may have enhanced the viability of the populations, but it did not save the species from regional extinction in the face of severe habitat loss and fragmentation. These results highlight a potentially common situation in changing environments: evolutionary changes are not strong enough to fully compensate for the direct adverse effects of environmental change and thereby rescue populations from extinction.
The number and demographic history of colonists can have dramatic consequences for the way in which genetic diversity is distributed and maintained in a metapopulation. The bed bug (Cimex lectularius) is a re-emerging pest species whose close association with humans has led to frequent local extinction and colonization, that is, to metapopulation dynamics. Pest control limits the lifespan of subpopulations, causing frequent local extinctions, and human-facilitated dispersal allows the colonization of empty patches. Founder events often result in drastic reductions in diversity and an increased influence of genetic drift. Coupled with restricted migration, this can lead to rapid population differentiation. We therefore predicted strong population structuring. Here, using 21 newly characterized microsatellite markers and approximate Bayesian computation (ABC), we investigate simplified versions of two classical models of metapopulation dynamics, in a coalescent framework, to estimate the number and genetic composition of founders in the common bed bug. We found very limited diversity within infestations but high degrees of structuring across the city of London, with extreme levels of genetic differentiation between infestations (FST = 0.59). ABC results suggest a common origin of all founders of a given subpopulation and that the numbers of colonists were low, implying that even a single mated female is enough to found a new infestation successfully. These patterns of colonization are close to the predictions of the propagule pool model, where all founders originate from the same parental infestation. These results show that aspects of metapopulation dynamics can be captured in simple models and provide insights that are valuable for the future targeted control of bed bug infestations.
Dispersal is important for determining both species ecological processes, such as population viability, and its evolutionary processes, like gene flow and local adaptation. Yet obtaining accurate estimates in the wild through direct observation can be challenging or even impossible, particularly over large spatial and temporal scales. Genotyping many individuals from wild populations can provide detailed inferences about dispersal. We therefore utilized genomewide marker data to estimate dispersal in the classic metapopulation of the Glanville fritillary butterfly (Melitaea cinxia L.), in the Åland Islands in SW Finland. This is an ideal system to test the effectiveness of this approach due to the wealth of information already available covering dispersal across small spatial and temporal scales, but lack of information at larger spatial and temporal scales. We sampled three larvae per larval family group from 3732 groups over a six‐year period and genotyped for 272 SNPs across the genome. We used this empirical data set to reconstruct cases where full‐sibs were detected in different local populations to infer female effective dispersal distance, that is, dispersal events directly contributing to gene flow. On average this was one kilometre, closely matching previous dispersal estimates made using direct observation. To evaluate our power to detect full‐sib families, we performed forward simulations using an individual‐based model constructed and parameterized for the Glanville fritillary metapopulation. Using these simulations, 100% of predicted full‐sibs were correct and over 98% of all true full‐sib pairs were detected. We therefore demonstrate that even in a highly dynamic system with a relatively small number of markers, we can accurately reconstruct full‐sib families and for the first time make inferences on female effective dispersal. This highlights the utility of this approach in systems where it has previously been impossible to obtain accurate estimates of dispersal over both ecological and evolutionary scales.
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