On the accumulation of deleterious mutations during range expansions

Peischl, Stephan; Dupanloup, Isabelle; Kirkpatrick, Mark; Excoffier, Laurent

doi:10.1111/mec.12524

Cited by 316 publications

(537 citation statements)

References 83 publications

(197 reference statements)

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“…Some studies showed similar numbers of putatively deleterious alleles per individual across human populations (3,4). In contrast, other recent studies reported a significant increase in the number of deleterious alleles (5, 37) and a higher additive genetic load in non-African populations compared with African populations (5,6,8,37,38). Our present findings of a higher genetic load in dogs compared with wolves supports the view that recent demographic history can affect genetic load.…”

Section: Significancecontrasting

confidence: 53%

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Bottlenecks and selective sweeps during domestication have increased deleterious genetic variation in dogs

Marsden

Vecchyo

O’Brien

et al. 2015

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

295

348

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Population bottlenecks, inbreeding, and artificial selection can all, in principle, influence levels of deleterious genetic variation. However, the relative importance of each of these effects on genome-wide patterns of deleterious variation remains controversial. Domestic and wild canids offer a powerful system to address the role of these factors in influencing deleterious variation because their history is dominated by known bottlenecks and intense artificial selection. Here, we assess genome-wide patterns of deleterious variation in 90 whole-genome sequences from breed dogs, village dogs, and gray wolves. We find that the ratio of amino acid changing heterozygosity to silent heterozygosity is higher in dogs than in wolves and, on average, dogs have 2-3% higher genetic load than gray wolves. Multiple lines of evidence indicate this pattern is driven by less efficient natural selection due to bottlenecks associated with domestication and breed formation, rather than recent inbreeding. Further, we find regions of the genome implicated in selective sweeps are enriched for amino acid changing variants and Mendelian disease genes. To our knowledge, these results provide the first quantitative estimates of the increased burden of deleterious variants directly associated with domestication and have important implications for selective breeding programs and the conservation of rare and endangered species. Specifically, they highlight the costs associated with selective breeding and question the practice favoring the breeding of individuals that best fit breed standards. Our results also suggest that maintaining a large population size, rather than just avoiding inbreeding, is a critical factor for preventing the accumulation of deleterious variants.M any of the mutations that arise in genomes are weakly deleterious and reduce fitness but are not always eliminated from the population by purifying natural selection. Consequently, understanding the reasons why deleterious mutations persist in populations and the role of demographic history in this process is of considerable interest (1-9). The radiation of domestic dogs offers a unique opportunity to address these questions. Dogs were originally domesticated from ancestral gray wolf populations >15,000 y ago in a process involving one or more severe population bottlenecks (10-12). The more recent isolation of modern dog breeds, which occurred over the last 300 y, involved additional population bottlenecks, intense artificial selection, and inbreeding Fig. 1A). Although this history is predicted to have resulted in the accumulation of deleterious variants, its specific effect on genomewide patterns of deleterious variation remains unclear.Here, we use complete genome sequencing data from 46 dogs representing 34 breeds, 25 village dogs, and 19 wolves to directly examine patterns of deleterious genetic variation across the dog genome (Dataset S1). Because more than half of these data derive from our own sequencing efforts, this project represents the largest survey of dog...

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Section: Significancecontrasting

confidence: 53%

“…Consequently, understanding the reasons why deleterious mutations persist in populations and the role of demographic history in this process is of considerable interest (1)(2)(3)(4)(5)(6)(7)(8)(9). The radiation of domestic dogs offers a unique opportunity to address these questions.…”

mentioning

confidence: 99%

Bottlenecks and selective sweeps during domestication have increased deleterious genetic variation in dogs

Marsden

Vecchyo

O’Brien

et al. 2015

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

295

348

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“…Given sufficient time, then, an optimal strategy on the invasion front would be to reallocate resources from competitive ability and towards dispersal [3]. How often, and indeed whether, this optimal strategy emerges on invasion fronts (where stochastic forces often lead to nonoptimal phenotypes dominating: [24][25][26]) is yet to be clarified with empirical studies. In our simulations, the effectiveness of a landscape barrier was very sensitive to the degree of long-distance dispersal.…”

Section: Discussionmentioning

confidence: 99%

“…B 283: 20153037 [35,36], enhanced kin competition [37], spatial sorting [38] and enhanced spatial selection [39] come into play. Mutation surfing can undermine fitness directly [24][25][26], while spatial sorting, enhanced spatial selection and kin competition work to fashion a phenotype that is adept at rapid dispersal, even if that dispersal enforces compromises in traits that enhance fitness in equilibrium populations [3]. By translocating range core individuals to the range edge, we eliminate the evolutionary conditions of the invasion front (the density gradient that drives spatial sorting as well as the high relatedness driving kin-competition effects), and bring invasion front phenotypes into direct conflict with fitter range core phenotypes.…”

Section: Discussionmentioning

confidence: 99%

The genetic backburn: using rapid evolution to halt invasions

2016

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The impact of an invasive species depends upon the extent of area across which it ultimately spreads. A powerful strategy for limiting impact, then, is to limit spread, and this can most easily be achieved by managing or reinforcing natural barriers to spread. Using a simulation model, we show that rapid evolutionary increases in dispersal can render permeable an otherwise effective barrier. On the other hand, we also show that, once the barrier is reached, and if it holds, resultant evolutionary decreases in dispersal rapidly make the barrier more effective. Finally, we sketch a strategy-the genetic backburn-in which low-dispersal individuals from the range core are translocated to the nearside of the barrier ahead of the oncoming invasion. We find that the genetic backburn-by preventing invasion front genotypes reaching the barrier, and hastening the evolutionary decrease in dispersal-can make barriers substantially more effective. In our simulations, the genetic backburn never reduced barrier strength, however, the improvement to barrier strength was negligible when there was substantial long-distance dispersal, or when there was no genetic variation for dispersal distance. The improvement in barrier strength also depended on the trade-off between dispersal and competitive ability, with a stronger trade-off conferring greater power to the genetic backburn.

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“…Nonetheless, there has long been interest in using spatial models for understanding processes underlying geographical variation in genetic polymorphisms (Wright, 1946;Kimura and Weiss, 1964). Spatial genetic models that investigate spatial and temporal dynamics remain an active area of research in population genetics (see for example Pieschl et al, 2013) and are becoming increasingly useful with the widespread availability of genome-scale data and computational power to generate more complex and realistic models that better reflect biological reality (Gompert et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

Demographic inference under a spatially continuous coalescent model

2016

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In contrast with the classical population genetics theory that models population structure as discrete panmictic units connected by migration, many populations exhibit heterogeneous spatial gradients in population connectivity across semi-continuous habitats. The historical dynamics of such spatially structured populations can be captured by a spatially explicit coalescent model recently proposed by Etheridge (2008) and Barton et al. (2010a, b) and whereby allelic lineages are distributed in a twodimensional spatial continuum and move within this continuum based on extinction and coalescent events. Though theoretically rigorous, this model, which we here refer to as the continuum model, has not yet been implemented for demographic inference. To this end, here we introduce and demonstrate a statistical pipeline that couples the coalescent simulator of Kelleher et al. (2014) that simulates genealogies under the continuum model, with an approximate Bayesian computation (ABC) framework for parameter estimation of neighborhood size (that is, the number of locally breeding individuals) and dispersal ability (that is, the distance an offspring can travel within a generation). Using empirically informed simulations and simulation-based ABC crossvalidation, we first show that neighborhood size can be accurately estimated. We then apply our pipeline to the South African endemic shrub species Berkheya cuneata to use the resulting estimates of dispersal ability and neighborhood size to infer the average population density of the species. More generally, we show that spatially explicit coalescent models can be successfully integrated into model-based demographic inference.

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On the accumulation of deleterious mutations during range expansions

Cited by 316 publications

References 83 publications

Bottlenecks and selective sweeps during domestication have increased deleterious genetic variation in dogs

Bottlenecks and selective sweeps during domestication have increased deleterious genetic variation in dogs

The genetic backburn: using rapid evolution to halt invasions

Demographic inference under a spatially continuous coalescent model

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