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The genomic impact of historical hybridization with massive mitochondrial DNA introgression.

ABSTRACT: BACKGROUND:The extent to which selection determines interspecific patterns of genetic exchange enlightens the role of adaptation in evolution and speciation. Often reported extensive interspecific introgression could be selection-driven, but also result from demographic processes, especially in cases of invasive species replacements, which can promote introgression at their invasion front. Because invasion and selective sweeps similarly mold variation, population genetics evidence for selection can only be gathered in an explicit demographic framework. The Iberian hare, Lepus granatensis, displays in its northern range extensive mitochondrial DNA introgression from L. timidus, an arctic/boreal species that it replaced locally after the last glacial maximum. We use whole-genome sequencing to infer geographic and genomic patterns of nuclear introgression and fit a neutral model of species replacement with hybridization, allowing us to evaluate how selection influenced introgression genome-wide, including for mtDNA. RESULTS:Although the average nuclear and mtDNA introgression patterns contrast strongly, they fit a single demographic model of post-glacial invasive replacement of timidus by granatensis. Outliers of elevated introgression include several genes related to immunity, spermatogenesis, and mitochondrial metabolism. Introgression is reduced on the X chromosome and in low recombining regions. CONCLUSIONS:General nuclear and mtDNA patterns of introgression can be explained by purely demographic processes. Hybrid incompatibilities and interplay between selection and recombination locally modulate levels of nuclear introgression. Selection promoted introgression of some genes involved in conflicts, either interspecific (parasites) or possibly cytonuclear. In the latter case, nuclear introgression could mitigate the potential negative effects of alien mtDNA on mitochondrial metabolism and male-specific traits.

SUBMITTER: Seixas FA

PROVIDER: S-EPMC6065068 | biostudies-literature | 2018 Jul

REPOSITORIES: biostudies-literature

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The genomic impact of historical hybridization with massive mitochondrial DNA introgression.

Seixas Fernando A FA Boursot Pierre P Melo-Ferreira José J

Genome biology 20180730 1

<h4>Background</h4>The extent to which selection determines interspecific patterns of genetic exchange enlightens the role of adaptation in evolution and speciation. Often reported extensive interspecific introgression could be selection-driven, but also result from demographic processes, especially in cases of invasive species replacements, which can promote introgression at their invasion front. Because invasion and selective sweeps similarly mold variation, population genetics evidence for se ...[more]

PMID: 30056805

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Project description:BackgroundEvidence of introgression, the transfer of genetic material, between crops and their wild relatives through spontaneous hybridization and subsequent backcrossing has been documented; however, the evolutionary patterns and consequences of introgression and its influence on the processes of crop domestication and varietal diversification are poorly understood.ResultsWe investigate the genomic landscape and evolution of putative crop-wild-relative introgression by analyzing the nuclear and chloroplast genomes from a panel of wild (Glycine soja) and domesticated (Glycine max) soybeans. Our data suggest that naturally occurring introgression between wild and domesticated soybeans was widespread and that introgressed variation in both wild and domesticated soybeans was selected against throughout the genomes and preferentially removed from the genomic regions underlying selective sweeps and domestication quantitative trait locus (QTL). In both taxa, putative introgression was preferentially retained in recombination-repressed pericentromeric regions that exhibit lower gene densities, reflecting potential roles of recombination in purging introgression. Despite extensive removal of introgressed variation by recurrent selection for domestication-related QTL and associated genomic regions, spontaneous interspecific hybridization during soybean domestication appear to have contributed to a rapid varietal diversification with high levels of genetic diversity and asymmetric evolution between the nuclear and chloroplast genomes.ConclusionsThis work reveals the evolutionary forces, patterns, and consequences of putative genomic introgression between crops and their wild relatives, and the effects of introgression on the processes of crop domestication and varietal diversification. We envision that interspecific introgression serves as an important mechanism for counteracting the reduction of genetic diversity in domesticated crops, particularly the ones under single domestication.

Project description:BACKGROUND:Genetic exchange in Trypanosoma cruzi is controversial not only in relation to its frequency, but also to its mechanism. Parasexual genetic exchange has been proposed based on laboratory hybrids, but population genomics strongly suggests meiosis in T. cruzi. In addition, mitochondrial introgression has been reported several times in natural isolates although its mechanism is not fully understood yet. Moreover, hybrid T. cruzi DTUs (TcV and TcVI) have inherited at least part of the kinetoplastic DNA (kDNA = mitochondrial DNA) from both parents. METHODOLOGY/PRINCIPAL FINDINGS:In order to address such topics, we sequenced and analyzed fourteen nuclear DNA fragments and three kDNA maxicircle genes in three TcI stocks which are natural clones potentially involved in events of genetic exchange. We also deep-sequenced (a total of 6,146,686 paired-end reads) the minicircle hypervariable region (mHVR) of the kDNA in such three strains. In addition, we analyzed the DNA content by flow cytometry to address cell ploidy. We observed that most polymorphic sites in nuclear loci showed a hybrid pattern in one cloned strain and the other two cloned strains were compatible as parental strains (or nearly related to the true parents). The three clones had almost the same ploidy and the DNA content was similar to the reference strain Sylvio (a nearly diploid strain). Despite maxicircle genes evolve faster than nuclear housekeeping ones, we detected no polymorphisms in the sequence of three maxicircle genes showing mito-nuclear discordance. Lastly, the hybrid stock shared 66% of its mHVR clusters with one putative parent and 47% with the other one; in contrast, the putative parental stocks shared less than 30% of the mHVR clusters between them. CONCLUSIONS/SIGNIFICANCE:The results suggest a reductive division, a natural hybridization, biparental inheritance of the minicircles in the hybrid and maxicircle introgression. The models including such phenomena and explaining the relationships between these three clones are discussed.

Project description:BACKGROUND:Introgression of mitochondrial DNA (mtDNA) is among the most frequently described cases of reticulate evolution. The tendency of mtDNA to cross interspecific barriers is somewhat counter-intuitive considering the key function of enzymes that it encodes in the oxidative-phosphorylation process, which could give rise to hybrid dysfunction. How mtDNA reticulation affects the evolution of metabolic functions is, however, uncertain. Here we investigated how morpho-physiological traits vary in natural populations of a common rodent (the bank vole, Myodes glareolus) and whether this variation could be associated with mtDNA introgression. First, we confirmed that M. glareolus harbour mtDNA introgressed from M. rutilus by analyzing mtDNA (cytochrome b, 954 bp) and nuclear DNA (four markers; 2333 bp in total) sequence variation and reconstructing loci phylogenies among six natural populations in Finland. We then studied geographic variation in body size and basal metabolic rate (BMR) among the populations of M. glareolus and tested its relationship with mtDNA type. RESULTS:Myodes glareolus and its arctic neighbour, M. rutilus, are reciprocally monophyletic at the analyzed nuclear DNA loci. In contrast, the two northernmost populations of M. glareolus have a fixed mitotype that is shared with M. rutilus, likely due to introgressive hybridization. The analyses of phenotypic traits revealed that the body mass and whole-body, but not mass corrected, BMR are significantly reduced in M. glareolus females from northern Finland that also have the introgressed mitotype. Restricting the analysis to the single population where the mitotypes coexist, the association of mtDNA type with whole-body BMR remained but those with mass corrected BMR and body mass did not. Mitochondrial sequence variation in the introgressed haplotypes is compatible with demographic growth of the populations, but may also be a result of positive selection. CONCLUSION:Our results show that the phenotypic traits vary markedly along the north-south axis of populations of M. glareolus. This variation may be related to adaptation to local environments and coincides with the gradient of genome reticulation between M. glareolus and M. rutilus, which was assessed by mtDNA introgression. Introgression of mtDNA may have affected morpho-physiological traits but do not show strong effects on either body mass or basal metabolic rate alone. We discuss the causes and biological meaning of our results and the means to clarify these questions in future research.

Project description:Siberian taimen Hucho taimen is the largest representative of the family Salmonidae inhabiting rivers of northern Eurasia. The species is under intensive aquaculture activity. To monitor natural taimen populations we have sequenced a portion (8,141 bp) of the mitochondrial (mt) genome in 28 specimens of H. taimen from six localities in the Amur River basin. Nucleotide variability is low (π = 0.0010), but structured in two divergent haplotype groups. A comparison of the data with the GenBank H. taimen mt genome (HQ897271) reveals significant differences between them in spite of the fact that the fish specimens come from neighboring geographical areas. The distribution of divergence is non-uniform with two highly pronounced divergent regions centered on two genes, ND3 and ND6. To clarify the pattern of divergence we sequenced the corresponding portion of the mt genome of lenok Brachymystax tumensis and analyzed the GenBank complete mt genomes of related species. We have found that the first and second divergent regions are identical between the GenBank H. taimen and two lenok subspecies, B. lenok and B. lenok tsinlingensis, respectively. Consequently, both divergent regions represent introgressed mtDNA resulting from intergeneric hybridization between the two lenok subspecies and H. taimen. Introgression is, however, not detected in our specimens. This plus the precise identity of the introgressed fragments between the donor and the recipient GenBank sequence suggests that the introgression is local and very recent, probably due to artificial manipulations involving taimen-lenok intergeneric hybridization. Human-mediated hybridization may become a major threat to aquatic biodiversity. Consequently we suggest that due attention needs to be given to this threat by means of responsible breeding program management, so as to prevent a potential spread of hybrid fishes that could jeopardize the resilience of locally adapted gene pools of the native H. taimen populations.

Dataset Information

The genomic impact of historical hybridization with massive mitochondrial DNA introgression.

Publications

The genomic impact of historical hybridization with massive mitochondrial DNA introgression.

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