Supergene formation is associated with a major shift in genome-wide patterns of diversity in a butterfly

AbstractSelection shapes genetic diversity around target mutations, yet little is known about how selection on specific loci affects the genetic trajectories of populations, including their genome-wide patterns of diversity and demographic responses. Adaptive introgression provides a way to assess how adaptive evolution at one locus impacts whole-genome biology. Here we study the patterns of genetic variation and geographic structure in a neotropical butterfly, Heliconius numata, and its closely related allies in the so-called melpomene-silvaniform subclade. H. numata is known to have evolved a supergene via the introgression of an adaptive inversion about 2.2 million years ago, triggering a polymorphism maintained by balancing selection. This locus controls variation in wing patterns involved in mimicry associations with distinct groups of co-mimics, and butterflies show disassortative mate preferences and heterozygote advantage at this locus. We contrasted patterns of genetic diversity and structure 1) among extant polymorphic and monomorphic populations of H. numata, 2) between H. numata and its close relatives, and 3) between ancestral lineages in a phylogenetic framework. We show that H. numata populations which carry the introgressed inversions in a balanced polymorphism show markedly distinct patterns of diversity compared to all other taxa. They show the highest diversity and demographic estimates in the entire clade, as well as a remarkably low level of geographic structure and isolation by distance across the entire Amazon basin. By contrast, monomorphic populations of H. numata as well as its sister species and their ancestral lineages all show the lowest effective population sizes and genetic diversity in the clade, and higher levels of geographical structure across the continent. This suggests that the large effective population size of polymorphic populations could be a property associated with harbouring the supergene. Our results are consistent with the hypothesis that the adaptive introgression of the inversion triggered a shift from directional to balancing selection and a change in gene flow due to disassortative mating, causing a general increase in genetic diversity and the homogenisation of genomes at the continental scale.

Download Full-text

Transition from background selection to associative overdominance promotes diversity in regions of low recombination

10.1101/748004 ◽

2019 ◽

Cited By ~ 5

Author(s):

Kimberly J. Gilbert ◽

Fanny Pouyet ◽

Laurent Excoffier ◽

Stephan Peischl

Keyword(s):

Genetic Diversity ◽

Balancing Selection ◽

Purifying Selection ◽

Heterozygote Advantage ◽

Background Selection ◽

Deleterious Mutations ◽

Recombination Rates ◽

Locus Model ◽

Genome Wide ◽

Linked Selection

SummaryLinked selection is a major driver of genetic diversity. Selection against deleterious mutations removes linked neutral diversity (background selection, BGS, Charlesworth et al. 1993), creating a positive correlation between recombination rates and genetic diversity. Purifying selection against recessive variants, however, can also lead to associative overdominance (AOD, Ohta 1971, Zhao & Charlesworth, 2016), due to an apparent heterozygote advantage at linked neutral loci that opposes the loss of neutral diversity by BGS. Zhao & Charlesworth (2016) identified the conditions when AOD should dominate over BGS in a single-locus model and suggested that the effect of AOD could become stronger if multiple linked deleterious variants co-segregate. We present a model describing how and under which conditions multi-locus dynamics can amplify the effects of AOD. We derive the conditions for a transition from BGS to AOD due to pseudo-overdominance (Ohta & Kimura 1970), i.e. a form of balancing selection that maintains complementary deleterious haplotypes that mask the effect of recessive deleterious mutations. Simulations confirm these findings and show that multi-locus AOD can increase diversity in low recombination regions much more strongly than previously appreciated. While BGS is known to drive genome-wide diversity in humans (Pouyet et al. 2018), the observation of a resurgence of genetic diversity in regions of very low recombination is indicative of AOD. We identify 21 such regions in the human genome showing clear signals of multi-locus AOD. Our results demonstrate that AOD may play an important role in the evolution of low recombination regions of many species.

Download Full-text

Heterogeneity in effective size across the genome: effects on the Inverse Instantaneous Coalescence Rate (IICR) and implications for demographic inference under linked selection.

10.1101/2021.06.11.448122 ◽

2021 ◽

Author(s):

Simon Boitard ◽

Armando Arredondo ◽

Camille Noûs ◽

Lounes Chikhi ◽

Olivier Mazet

Keyword(s):

Genetic Diversity ◽

Balancing Selection ◽

Effective Population ◽

Recombination Rates ◽

Genome Wide ◽

Coalescence Rate ◽

Demographic Inference ◽

The Impact ◽

Linked Selection ◽

Coalescence Times

The relative contribution of selection and neutrality in shaping species genetic diversity is one of the most central and controversial questions in evolutionary theory. Genomic data provide growing evidence that linked selection, i.e. the modification of genetic diversity at neutral sites through linkage with selected sites, might be pervasive over the genome. Several studies proposed that linked selection could be modelled as first approximation by a local reduction (e.g. purifying selection, selective sweeps) or increase (e.g. balancing selection) of effective population size (Ne). At the genome-wide scale, this leads to a large variance of Ne from one region to another, reflecting the heterogeneity of selective constraints and recombination rates between regions. We investigate here the consequences of this variation of Ne on the genome-wide distribution of coalescence times. The underlying motivation concerns the impact of linked selection on demographic inference, because the distribution of coalescence times is at the heart of several important demographic inference approaches. Using the concept of Inverse Instantaneous Coalescence Rate, we demonstrate that in a panmictic population, linked selection always results in a spurious apparent decrease of Ne along time. Balancing selection has a particularly large effect, even when it concerns a very small part of the genome. We quantify the expected magnitude of the spurious decrease of Ne in humans and Drosophila melanogaster, based on Ne distributions inferred from real data in these species. We also find that the effect of linked selection can be significantly reduced by that of population structure.

Download Full-text

Genomics of sorghum local adaptation to a parasitic plant

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1908707117 ◽

2020 ◽

Vol 117 (8) ◽

pp. 4243-4251 ◽

Cited By ~ 3

Author(s):

Emily S. Bellis ◽

Elizabeth A. Kelly ◽

Claire M. Lorts ◽

Huirong Gao ◽

Victoria L. DeLeo ◽

...

Keyword(s):

Genetic Diversity ◽

Local Adaptation ◽

Species Interactions ◽

Balancing Selection ◽

Control Plant ◽

Farming Systems ◽

Striga Hermonthica ◽

Loss Of Function ◽

Trade Offs ◽

Genome Wide

Host–parasite coevolution can maintain high levels of genetic diversity in traits involved in species interactions. In many systems, host traits exploited by parasites are constrained by use in other functions, leading to complex selective pressures across space and time. Here, we study genome-wide variation in the staple crop Sorghum bicolor (L.) Moench and its association with the parasitic weed Striga hermonthica (Delile) Benth., a major constraint to food security in Africa. We hypothesize that geographic selection mosaics across gradients of parasite occurrence maintain genetic diversity in sorghum landrace resistance. Suggesting a role in local adaptation to parasite pressure, multiple independent loss-of-function alleles at sorghum LOW GERMINATION STIMULANT 1 (LGS1) are broadly distributed among African landraces and geographically associated with S. hermonthica occurrence. However, low frequency of these alleles within S. hermonthica-prone regions and their absence elsewhere implicate potential trade-offs restricting their fixation. LGS1 is thought to cause resistance by changing stereochemistry of strigolactones, hormones that control plant architecture and below-ground signaling to mycorrhizae and are required to stimulate parasite germination. Consistent with trade-offs, we find signatures of balancing selection surrounding LGS1 and other candidates from analysis of genome-wide associations with parasite distribution. Experiments with CRISPR–Cas9-edited sorghum further indicate that the benefit of LGS1-mediated resistance strongly depends on parasite genotype and abiotic environment and comes at the cost of reduced photosystem gene expression. Our study demonstrates long-term maintenance of diversity in host resistance genes across smallholder agroecosystems, providing a valuable comparison to both industrial farming systems and natural communities.

Download Full-text

Challenges to assessing connectivity between massive populations of the Australian plague locust

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2010.2605 ◽

2011 ◽

Vol 278 (1721) ◽

pp. 3152-3160 ◽

Cited By ~ 24

Author(s):

Marie-Pierre Chapuis ◽

Julie-Anne M. Popple ◽

Karine Berthier ◽

Stephen J. Simpson ◽

Edward Deveson ◽

...

Keyword(s):

Genetic Diversity ◽

Large Population ◽

Movement Ecology ◽

Effective Population ◽

Continental Scale ◽

Australian Continent ◽

Population Structuring ◽

Population Sizes ◽

Approximate Bayesian ◽

Australian Plague Locust

Linking demographic and genetic dispersal measures is of fundamental importance for movement ecology and evolution. However, such integration can be difficult, particularly for highly fecund species that are often the target of management decisions guided by an understanding of population movement. Here, we present an example of how the influence of large population sizes can preclude genetic approaches from assessing demographic population structuring, even at a continental scale. The Australian plague locust, Chortoicetes terminifera , is a significant pest, with populations on the eastern and western sides of Australia having been monitored and managed independently to date. We used microsatellites to assess genetic variation in 12 C. terminifera population samples separated by up to 3000 km. Traditional summary statistics indicated high levels of genetic diversity and a surprising lack of population structure across the entire range. An approximate Bayesian computation treatment indicated that levels of genetic diversity in C. terminifera corresponded to effective population sizes conservatively composed of tens of thousands to several million individuals. We used these estimates and computer simulations to estimate the minimum rate of dispersal, m , that could account for the observed range-wide genetic homogeneity. The rate of dispersal between both sides of the Australian continent could be several orders of magnitude lower than that typically considered as required for the demographic connectivity of populations.

Download Full-text

Linkage disequilibrium and within-breed genetic diversity in Iranian Zandi sheep

Archives Animal Breeding ◽

10.5194/aab-62-143-2019 ◽

2019 ◽

Vol 62 (1) ◽

pp. 143-151 ◽

Cited By ~ 6

Author(s):

Seyed Mohammad Ghoreishifar ◽

Hossein Moradi-Shahrbabak ◽

Nahid Parna ◽

Pourya Davoudi ◽

Majid Khansefid

Keyword(s):

Genetic Diversity ◽

Linkage Disequilibrium ◽

Association Studies ◽

Genome Wide Association Studies ◽

Effective Population ◽

High Genetic Diversity ◽

Single Nucleotide ◽

Genome Wide ◽

Snp Panel ◽

Zandi Sheep

Abstract. This research aimed to measure the extent of linkage disequilibrium (LD), effective population size (Ne), and runs of homozygosity (ROHs) in one of the major Iranian sheep breeds (Zandi) using 96 samples genotyped with Illumina Ovine SNP50 BeadChip. The amount of LD (r2) for single-nucleotide polymorphism (SNP) pairs in short distances (10–20 kb) was 0.21±0.25 but rapidly decreased to 0.10±0.16 by increasing the distance between SNP pairs (40–60 kb). The Ne of Zandi sheep in past (approximately 3500 generations ago) and recent (five generations ago) populations was estimated to be 6475 and 122, respectively. The ROH-based inbreeding was 0.023. We found 558 ROH regions, of which 37 % were relatively long (> 10 Mb). Compared with the rate of LD reduction in other species (e.g., cattle and pigs), in Zandi, it was reduced more rapidly by increasing the distance between SNP pairs. According to the LD pattern and high genetic diversity of Zandi sheep, we need to use an SNP panel with a higher density than Illumina Ovine SNP50 BeadChip for genomic selection and genome-wide association studies in this breed.

Download Full-text

The role of infectious disease, inbreeding and mating preferences in maintaining MHC genetic diversity: an experimental test

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.1994.0154 ◽

1994 ◽

Vol 346 (1317) ◽

pp. 369-378 ◽

Cited By ~ 92

Keyword(s):

Genetic Diversity ◽

Balancing Selection ◽

Natural Populations ◽

House Mice ◽

Heterozygote Advantage ◽

Immune Recognition ◽

Mating Preferences ◽

Conventional View ◽

Mhc Genes ◽

Allele Specific

In house mice, and probably most mammals, major histocompatibility complex (MHC) gene products influence both immune recognition and individual odours in an allele-specific fashion. Although it is generally assumed that some form of pathogen-driven balancing selection is responsible for the unprecedented genetic diversity of MHC genes, the MHC-based mating preferences observed in house mice are sufficient to account for the genetic diversity of MHC genes found in this and other vertebrates. These MHC disassortative mating preferences are completely consistent with the conventional view that pathogen-driven MHC heterozygote advantage operates on MHC genes. This is because such matings preferentially produce MHC-heterozygours progeny, which could enjoy enhanced disease resistance. However, such matings could also function to avoid genome-wide inbreeding. To discriminate between these two hypotheses we measured the fitness consequences of both experimentally manipulated levels of inbreeding and MHC homozygosity and heterozygosity in semi-natural populations of wild-derived house mice. We were able to measure a fitness decline associated with inbreeding, but were unable to detect fitness declines associated with MHC homozygosity. These data suggest that inbreeding avoidance may be the most important function of MHC-based mating preferences and therefore the fundamental selective force diversifying MHC genes in species with such mating patterns. Although controversial, this conclusion is consistent with the majority of the data from the inbreeding and immunological literature.

Download Full-text

Low genetic variation is associated with low mutation rate in the giant duckweed

10.1101/381574 ◽

2018 ◽

Cited By ~ 1

Author(s):

Shuqing Xu ◽

Jessica Stapley ◽

Saskia Gablenz ◽

Justin Boyer ◽

Klaus J. Appenroth ◽

...

Keyword(s):

Genetic Diversity ◽

Population Size ◽

Mutation Rate ◽

Spontaneous Mutation ◽

Effective Population ◽

Spontaneous Mutation Rate ◽

Low Genetic Diversity ◽

Genome Wide ◽

Census Population Size

AbstractMutation rate and effective population size (Ne) jointly determine intraspecific genetic diversity, but the role of mutation rate is often ignored. We investigate genetic diversity, spontaneous mutation rate andNein the giant duckweed (Spirodela polyrhiza). Despite its large census population size, whole-genome sequencing of 68 globally sampled individuals revealed extremely low within-species genetic diversity. Assessed under natural conditions, the genome-wide spontaneous mutation rate is at least seven times lower than estimates made for other multicellular eukaryotes, whereasNeis large. These results demonstrate that low genetic diversity can be associated with large-Nespecies, where selection can reduce mutation rates to very low levels, and accurate estimates of mutation rate can help to explain seemingly counterintuitive patterns of genome-wide variation.One Sentence SummaryThe low-down on a tiny plant: extremely low genetic diversity in an aquatic plant is associated with its exceptionally low mutation rate.

Download Full-text

Genome-wide Single Nucleotide Polymorphism Analyses Reveal Genetic Diversity and Structure of Wild and Domestic Cattle in Bangladesh

Asian-Australasian Journal of Animal Sciences ◽

10.5713/ajas.2014.14160 ◽

2014 ◽

Vol 27 (10) ◽

pp. 1381-1386 ◽

Cited By ~ 10

Author(s):

Md. Rasel Uzzaman ◽

Zewdu Edea ◽

Md. Shamsul Alam Bhuiyan ◽

Jeremy Walker ◽

A. K. F. H. Bhuiyan ◽

...

Keyword(s):

Genetic Diversity ◽

Single Nucleotide Polymorphism ◽

Nucleotide Polymorphism ◽

Single Nucleotide ◽

Genome Wide ◽

Genetic Diversity And Structure

Download Full-text

Demography and natural selection have shaped genome-wide variation in the widely distributed conifer Norway Spruce (Picea abies)

10.1101/805903 ◽

2019 ◽

Author(s):

Xi Wang ◽

Carolina Bernhardsson ◽

Pär K. Ingvarsson

Keyword(s):

Genetic Diversity ◽

Natural Selection ◽

Picea Abies ◽

Population Size ◽

Effective Population Size ◽

Norway Spruce ◽

Demographic History ◽

Sequencing Data ◽

Effective Population ◽

Genome Wide

AbstractUnder the neutral theory, species with larger effective population sizes are expected to harbour higher genetic diversity. However, across a wide variety of organisms, the range of genetic diversity is orders of magnitude more narrow than the range of effective population size. This observation has become known as Lewontin’s paradox and although aspects of this phenomenon have been extensively studied, the underlying causes for the paradox remain unclear. Norway spruce (Picea abies) is a widely distributed conifer species across the northern hemisphere and it consequently plays a major role in European forestry. Here, we use whole-genome re-sequencing data from 35 individuals to perform population genomic analyses in P. abies in an effort to understand what drives genome-wide patterns of variation in this species. Despite having a very wide geographic distribution and an enormous current population size, our analyses find that genetic diversity of P.abies is low across a number of populations (p=0.005-0.006). To assess the reasons for the low levels of genetic diversity, we infer the demographic history of the species and find that it is characterised by several re-occurring bottlenecks with concomitant decreases in effective population size can, at least partly, provide an explanation for low polymorphism we observe in P. abies. Further analyses suggest that recurrent natural selection, both purifying and positive selection, can also contribute to the loss of genetic diversity in Norway spruce by reducing genetic diversity at linked sites. Finally, the overall low mutation rates seen in conifers can also help explain the low genetic diversity maintained in Norway spruce.

Download Full-text

Conservation genomic analysis reveals ancient introgression and declining levels of genetic diversity in Madagascar’s hibernating dwarf lemurs

10.1101/620724 ◽

2019 ◽

Cited By ~ 1

Author(s):

Rachel C. Williams ◽

Marina B. Blanco ◽

Jelmer W. Poelstra ◽

Kelsie E. Hunnicutt ◽

Aaron A. Comeault ◽

...

Keyword(s):

Genetic Diversity ◽

Genomic Analysis ◽

Population Level ◽

Comparative Genomic ◽

Effective Population ◽

High Coverage ◽

Genome Wide ◽

Conservation Concern ◽

Genomic Regions ◽

Dwarf Lemur

AbstractMadagascar’s biodiversity is notoriously threatened by deforestation and climate change. Many of these organisms are rare, cryptic, and severely threatened, making population-level sampling unrealistic. Such is the case with Madagascar’s dwarf lemurs (genus Cheirogaleus), the only obligate hibernating primate. We here apply comparative genomic approaches to generate the first genome-wide estimates of genetic diversity within dwarf lemurs. We generate a reference genome for the fat-tailed dwarf lemur, Cheirogaleus medius, and use this resource to facilitate analyses of high-coverage (~30x) genome sequences for wild-caught individuals representing species: C. sp. cf. medius, C. major, C. crossleyi and C. sibreei. This study represents the largest contribution to date of novel genomic resources for Madagascar’s lemurs. We find concordant phylogenetic relationships among the four lineages of Cheirogaleus across most of the genome, and yet detect a number of discordant genomic regions consistent with ancient admixture. We hypothesized that these regions could have resulted from adaptive introgression related to hibernation, indeed finding that genes associated with hibernation are present, though most significantly, that gene ontology categories relating to transcription are over-represented. We estimate levels of heterozygosity and find particularly low levels in an individual sampled from an isolated population of C. medius that we refer to as C. sp. cf. medius. Results are consistent with a recent decline in effective population size, which is evident across species. Our study highlights the power of comparative genomic analysis for identifying species and populations of conservation concern, as well as for illuminating possible mechanisms of adaptive phenotypic evolution.

Download Full-text