Reproductive isolation of hybrid populations driven by genetic incompatibilities.
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ABSTRACT:
SUBMITTER: Schumer M
PROVIDER: S-EPMC4359097 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Natural hybrid zones offer a powerful framework for understanding the genetic basis of speciation in progress because ongoing hybridization continually creates unfavorable gene combinations. Evidence indicates that postzygotic reproductive isolation is often caused by epistatic interactions between mutations in different genes that evolved independently of one another (hybrid incompatibilities). We examined the potential to detect epistatic selection against incompatibilities from genome sequence data using the site frequency spectrum (SFS) of polymorphisms by conducting individual-based simulations in SLiM. We found that the genome-wide SFS in hybrid populations assumes a diagnostic shape, with the continual input of fixed differences between source populations via migration inducing a mass at intermediate allele frequency. Epistatic selection locally distorts the SFS as non-incompatibility alleles rise in frequency in a manner analogous to a selective sweep. Building on these results, we present a statistical method to identify genomic regions containing incompatibility loci that locates departures in the local SFS compared with the genome-wide SFS. Cross-validation studies demonstrate that our method detects recessive and codominant incompatibilities across a range of scenarios varying in the strength of epistatic selection, migration rate, and hybrid zone age. Our approach takes advantage of whole genome sequence data, does not require knowledge of demographic history, and can be applied to any pair of nascent species that forms a hybrid zone.
| S-EPMC8476132 | biostudies-literature
Project description:Studying reproductive barriers between populations of the same species is critical to understand how speciation may proceed. Growing evidence suggests postmating, prezygotic (PMPZ) reproductive barriers play an important role in the evolution of early taxonomic divergence. However, the contribution of PMPZ isolation to speciation is typically studied between species in which barriers that maintain isolation may not be those that contributed to reduced gene flow between populations. Moreover, in internally fertilizing animals, PMPZ isolation is related to male ejaculate-female reproductive tract incompatibilities but few studies have examined how mating history of the sexes can affect the strength of PMPZ isolation and the extent to which PMPZ isolation is repeatable or restricted to particular interacting genotypes. We addressed these outstanding questions using multiple populations of Drosophila montana. We show a recurrent pattern of PMPZ isolation, with flies from one population exhibiting reproductive incompatibility in crosses with all three other populations, while those three populations were fully fertile with each other. Reproductive incompatibility is due to lack of fertilization and is asymmetrical, affecting female fitness more than males. There was no effect of male or female mating history on reproductive incompatibility, indicating that PMPZ isolation persists between populations. We found no evidence of variability in fertilization outcomes attributable to different female × male genotype interactions, and in combination with our other results, suggests that PMPZ isolation is not driven by idiosyncratic genotype × genotype interactions. Our results show PMPZ isolation as a strong, consistent barrier to gene flow early during speciation and suggest several targets of selection known to affect ejaculate-female reproductive tract interactions within species that may cause this PMPZ isolation.
| S-EPMC6157668 | biostudies-literature
Project description:Speciation is fundamental to the process of generating the huge diversity of life on Earth. However, we are yet to have a clear understanding of its molecular-genetic basis. Here, we examine a computational model of reproductive isolation that explicitly incorporates a map from genotype to phenotype based on the biophysics of protein-DNA binding. In particular, we model the binding of a protein transcription factor to a DNA binding site and how their independent coevolution, in a stabilizing fitness landscape, of two allopatric lineages leads to incompatibilities. Complementing our previous coarse-grained theoretical results, our simulations give a new prediction for the monomorphic regime of evolution that smaller populations should develop incompatibilities more quickly. This arises as (1) smaller populations have a greater initial drift load, as there are more sequences that bind poorly than well, so fewer substitutions are needed to reach incompatible regions of phenotype space, and (2) slower divergence when the population size is larger than the inverse of discrete differences in fitness. Further, we find longer sequences develop incompatibilities more quickly at small population sizes, but more slowly at large population sizes. The biophysical model thus represents a robust mechanism of rapid reproductive isolation for small populations and large sequences that does not require peak shifts or positive selection. Finally, we show that the growth of DMIs with time is quadratic for small populations, agreeing with Orr's model, but nonpower law for large populations, with a form consistent with our previous theoretical results.
| S-EPMC4676520 | biostudies-literature
Project description:Horizontal gene transfer and recombination play a major role in microbial evolution and have been detected in diverse groups, including many of medical relevance such as HIV and dengue virus. In the absence of mechanistic barriers, the evolutionary success of a particular recombination event is determined by whether the recombinant genotype suffers a fitness cost through the disruption of favorable epistatic interactions within the genome, and if so, the extent to which this fitness cost might be mitigated by subsequent compensatory evolution. To investigate the importance of epistatic interactions between genes and the evolutionary viability of a homologous recombination event between diverged ancestral genotypes, we constructed two recombinant microvirid bacteriophages by exchanging their alleles of the gene encoding the coat protein. The coding sequences for this gene differ by approximately 8% at the amino acid level and were interchanged between two ancestral phages related to varphiX174 and well adapted to their culture conditions. Because the recombinant phages showed drastically reduced fitnesses, we further explored their evolutionary viability by subjecting replicate lines of each of them to selection. We found that all four lineages achieved fitnesses commensurate with ancestral fitnesses in as few as 60 generations, and on average, the first substitution accounted for more than half of the total fitness recovery. Fitness recovery required three to five substitutions in each lineage, and overall eight of the nine essential phage genes were involved, suggesting extensive epistatic interactions throughout the genome. Interestingly, the proteins with the most extensive and apparent physical interactions with the exchanged protein in the viral capsid did not appear to have much of a role in fitness recovery. This result appears to be a consequence of the conservation of the amino acid residues involved in the interactions. It suggests that strong epistatic interactions are less important than weaker, transient ones in producing genic incompatibilities because they preclude variability in the interacting regions of the proteins.
| S-EPMC2912467 | biostudies-literature
Project description:A rickettsial bacterium in the genus Wolbachia is the cause of a unidirectional reproductive incompatibility observed between two major beetle pests of maize, the western corn rootworm, Diabrotica virgifera virgifera, and the Mexican corn rootworm, D. v. zeae. These subspecies are allopatric except for two known regions of sympatry in Texas and Mexico. We demonstrate that populations of D. v. virgifera, with the exception of two populations in southern Arizona, are infected with a strain of Wolbachia. Populations of D. v. zeae are not infected. Treatment of D. v. virgifera with tetracycline eliminated the Wolbachia and removed the reproductive incompatibility. Similar patterns of reproductive incompatibility exist among taxa of the cricket genus Gryllus. Gryllus assimilis, G. integer, G. ovisopis, G. pennsylvanicus, and G. rubens are infected with Wolbachia whereas G. firmus is usually not. Populations of G. rubens and G. ovisopis carry the same Wolbachia strain, which is distinct from that of G. integer. G. pennsylvanicus is infected with two Wolbachia strains, that found in G. rubens and one unique to G. pennsylvanicus. Moreover, a proportion of G. pennsylvanicus individuals harbors both strains. Wolbachia may have influenced speciation in some members of the genus Gryllus by affecting the degree of hybridization between species. Given that Wolbachia infections are relatively common in insects, it is likely that other insect hybrid zones may be influenced by infections with Wolbachia.
| S-EPMC23493 | biostudies-literature
Project description:Meiotically driving sex chromosomes manipulate gametogenesis to increase their transmission at a cost to the rest of the genome. The intragenomic conflicts they produce have major impacts on the ecology and evolution of their host species. However, their ecological dynamics remain poorly understood. Simple population genetic models predict meiotic drivers will rapidly reach fixation in populations and spread across landscapes. In contrast, natural populations commonly show spatial variation in the frequency of drivers, with drive present in clines or mosaics across species ranges. For example, Drosophila subobscura harbors a sex ratio distorting drive chromosome (SRs) at 15-25% frequency in North Africa, present at less than 2% frequency in adjacent southern Spain, and absent in other European populations. Here, we investigate the forces preventing the spread of the driver northward. We show that SRs has remained at a constant frequency in North Africa, and failed to spread in Spain. We find strong evidence that spread is impeded by genetic incompatibility between SRs and Spanish autosomal backgrounds. When we cross SRs from North Africa onto Spanish genetic backgrounds we observe strong incompatibilities specific to hybrids bearing SRs. The incompatibilities increase in severity in F2 male hybrids, leading to almost complete infertility. We find no evidence supporting an alternative hypothesis, that there is resistance to drive in Spanish populations. We conclude that the source of the stepped frequency variation is genetic incompatibility between the SRs chromosome and the genetic backgrounds of the adjacent population, preventing SRs spreading northward. The low frequency of SRs in South Spain is consistent with recurrent gene flow across the Strait of Gibraltar combined with selection against the SRs element through genetic incompatibility. This demonstrates that incompatibilities between drive chromosomes and naïve populations can prevent the spread of drive between populations, at a continental scale.
| S-EPMC6121854 | biostudies-other
Project description:Species pairs often become genetically incompatible during divergence, which is an important source of reproductive isolation. An idealized picture is often painted where incompatibility alleles accumulate and fix between diverging species. However, recent studies have shown both that incompatibilities can collapse with ongoing hybridization, and that incompatibility loci can be polymorphic within species. This paper suggests some general rules for the behavior of incompatibilities under hybridization. In particular, we argue that redundancy of genetic pathways can strongly affect the dynamics of intrinsic incompatibilities. Since fitness in genetically redundant systems is unaffected by introducing a few foreign alleles, higher redundancy decreases the stability of incompatibilities during hybridization, but also increases tolerance of incompatibility polymorphism within species. We use simulations and theories to show that this principle leads to two types of collapse: in redundant systems, exemplified by classical Dobzhansky-Muller incompatibilities, collapse is continuous and approaches a quasi-neutral polymorphism between broadly sympatric species, often as a result of isolation-by-distance. In nonredundant systems, exemplified by co-evolution among genetic elements, incompatibilities are often stable, but can collapse abruptly with spatial traveling waves. As both types are common, the proposed principle may be useful in understanding the abundance of genetic incompatibilities in natural populations.
| S-EPMC9827863 | biostudies-literature
Project description:BackgroundEvolution of reproductive isolation is an important process, generating biodiversity and driving speciation. To better understand this process, it is necessary to investigate factors underlying reproductive isolation through various approaches but also in various taxa. Previous studies, mainly focusing on diploid animals, supported the prevalent view that reproductive barriers evolve gradually as a by-product of genetic changes accumulated by natural selection by showing a positive relationship between the degree of reproductive isolation and genetic distance. Haplodiploid animals are expected to generate additional insight into speciation, but few studies investigated the prevalent view in haplodiploid animals. In this study, we investigate whether the relationship also holds in a haplodiploid spider mite, Amphitetranychus viennensis (Zacher).ResultsWe sampled seven populations of the mite in the Palaearctic region, measured their genetic distance (mtDNA) and carried out cross experiments with all combinations. We analyzed how lack of fertilization rate (as measure of prezygotic isolation) as well as hybrid inviability and hybrid sterility (as measures of postzygotic isolation) varies with genetic distance. We found that the degree of reproductive isolation varies among cross combinations, and that all three measures of reproductive isolation have a positive relationship with genetic distance. Based on the mtDNA marker, lack of fertilization rate, hybrid female inviability and hybrid female sterility were estimated to be nearly complete (99.0-99.9% barrier) at genetic distances of 0.475-0.657, 0.150-0.209 and 0.145-0.210, respectively. Besides, we found asymmetries in reproductive isolation.ConclusionsThe prevalent view on the evolution of reproductive barriers is supported in the haplodiploid spider mite we studied here. According to the estimated minimum genetic distance for total reproductive isolation in parent population crosses in this study and previous work, a genetic distance of 0.15-0.21 in mtDNA (COI) appears required for speciation in spider mites. Variations and asymmetries in the degree of reproductive isolation highlight the importance of reinforcement of prezygotic reproductive isolation through incompatibility and the importance of cytonuclear interactions for reproductive isolation in haplodiploid spider mites.
| S-EPMC8459536 | biostudies-literature
Project description:The piRNA pathway is an adaptive mechanism for maintaining the stability of the genome by repression selfish genomic elements such as transposons. As a host defense mechanism the piRNA pathway is rapidly evolving with different sets of piRNA silencing different targets in closely-related species. In male germline of D.melanogaster, repression of Stellate genes by piRNA generated from Supressor of Stellate, Su(Ste), locus is required for male fertility, but both Su(Ste) piRNA and their targets are absent in other Drosophila species. Here we showed that D.melanogaster genome contain non-coding genomic repeats that have sequence similarity to vasa, protein-coding host gene essential for germline development. In male germline Vasa Related (Varel) repeats produce abundant piRNA that are anti-sense to vasa, however, vasa mRNA escape silencing due to imperfect complementarity between piRNA and vasa sequences. Unexpectedly, we found that Varel piRNA of D.melanogaster target vasa of closely related D. mauritana species in interspecies hybrids. The same hybrids show derepression of harmful Stellate locus due to the absence of Su(Ste) piRNA. Thus, the piRNA pathway contributes to the reproductive isolation between Drosophila species, causing hybrid male sterility via misregulation of two different host factors.
2019-02-19 | GSE120802 | GEO
Project description:Bacterial investigation from Tetranychus populations
| PRJEB60422 | ENA