Gap genes are involved in inviability in hybrids between Drosophila melanogaster and D. santomea

ABSTRACTEvolved changes within species lead to the inevitable loss of viability in hybrids. Inviability is also a convenient phenotype to genetically map and validate functionally divergent genes and pathways differentiating closely related species. Here we identify the Drosophila melanogaster form of the highly conserved essential gap gene giant (gt) as a key genetic determinant of hybrid inviability in crosses with D. santomea. We show that the coding region of this allele in D. melanogaster/D. santomea hybrids is sufficient to cause embryonic inviability not seen in either pure species. Further genetic analysis indicates that tailless (tll), another gap gene, is also involved in the hybrid defects. giant and tll are both members of the gap gene network of transcription factors that participate in establishing anterior-posterior specification of the dipteran embryo, a highly conserved developmental process. Genes whose outputs in this process are functionally conserved nevertheless evolve over short timescales to cause inviability in hybrids.

Patterns of reproductive isolation in a haplodiploid mite, Amphitetranychus viennensis: prezygotic isolation, hybrid inviability and hybrid sterility

Background Evolution 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). Results We 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. Conclusions The 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.

Patterns of reproductive isolation in a haplodiploid mite, Amphitetranychus viennensis: prezygotic isolation, hybrid inviability and hybrid sterility

Background Evolution 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). Results We 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 0.138–0.204, respectively. Conclusions The 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 and previous studies, a genetic distance of 0.152–0.210 in mtDNA (COI) appears required for speciation in spider mites. Due to a lack of hybrid males, we could not address Haldane’s rule, which can be extended to haplodiploids, even though we focused on a young diverging group of spider mites. Our results highlight the importance of cytonuclear interactions for reproductive isolation in haplodiploid spider mites.

Haldane’s rule in the placenta: sex-biased misregulation of the Kcnq1 imprinting cluster in hybrid mice

ABSTRACTMammalian hybrids often show striking asymmetries in their phenotypes both between reciprocal crosses, and between sexes in accordance with Haldane’s rule. Hybrid inviability is associated with parent-of-origin placental growth abnormalities for which misregulation of imprinted genes is a strong candidate mechanism. However, direct evidence for the involvement of abnormal imprinting and the mechanisms behind this proposed misregulation is limited. We used transcriptome and reduced representation bisulfite sequencing to evaluate the contribution of imprinted genes to a long-standing example of parent-of-origin placental growth dysplasia in the cross between the house mouse (Mus musculus domesticus) and the Algerian mouse (Mus spretus). We found little evidence for loss of imprinting and imprinted genes with biallelic expression were not misexpressed. Instead, imprinted genes with transgressive expression and methylation were concentrated in the Kcnq1 cluster, which contains causal genes for prenatal growth abnormalities in both mice and humans. Hypermethylation of the cluster’s imprinting control region, and consequent misexpression of the genes Phlda2 and Ascl2, is a strong candidate mechanism for hybrid placental undergrowth. Transgressive placental and gene regulatory phenotypes, including expression and methylation in the Kcnq1 cluster, were more extreme in hybrid males. While consistent with Haldane’s rule, male-biased defects are not expected in rodent placenta because the maternal X chromosome is effectively hemizygous in both sexes. In search of an explanation we found evidence of leaky imprinted X-chromosome inactivation in hybrid females. Supplementary expression from the paternal X-chromosome may buffer the females from the effects of X-linked incompatibilities to which males are fully exposed. Sex differences in chromatin structure on the X and sex-biased maternal effects are non-mutually exclusive alternative explanations for adherence to Haldane’s rule in hybrid placenta. The results of this study contribute to understanding of the genetic basis of hybrid inviability in mammals, and the role of imprinted genes in speciation.

When acting as a reproductive barrier for sympatric speciation, hybrid sterility can only be primary

Animal gametes unite to form a zygote that develops into an adult with gonads that, in turn, produce gametes. Interruption of this germinal cycle by prezygotic or postzygotic reproductive barriers can result in two cycles, each with the potential to evolve into a new species. When the speciation process is complete, members of each species are fully reproductively isolated from those of the other. During speciation a primary barrier may be supported and eventually superceded by a later-appearing secondary barrier. For those holding certain cases of prezygotic isolation to be primary (e.g. elephant cannot copulate with mouse), the onus is to show that they had not been preceded over evolutionary time by periods of postzygotic hybrid inviability (genically determined) or sterility (genically or chromosomally determined). Likewise, the onus is upon those holding cases of hybrid inviability to be primary (e.g. Dobzhansky–Muller epistatic incompatibilities) to show that they had not been preceded by periods, however brief, of hybrid sterility. The latter, when acting as a sympatric barrier causing reproductive isolation, can only be primary. In many cases, hybrid sterility may result from incompatibilities between parental chromosomes that attempt to pair during meiosis in the gonad of their offspring (Winge-Crowther-Bateson incompatibilities). While such incompatibilities have long been observed on a microscopic scale, there is growing evidence for a role of dispersed finer DNA sequence differences (i.e. in base k-mers).

Patterns of hybrid seed inviability in perennials of the Mimulus guttatus sp. complex reveal a potential role of parental conflict in reproductive isolation

SummaryGenomic conflicts may play a central role in the evolution of reproductive barriers. Theory predicts that early-onset hybrid inviability may stem from conflict between parents for resource allocation to offspring. Here we describe M. decorus; a group of cryptic species within the M. guttatus species complex that are largely reproductively isolated by hybrid seed inviability (HSI). HSI between M. guttatus and M. decorus is common and strong, but populations of M. decorus vary in the magnitude and directionality of HSI with M. guttatus. Patterns of HSI between M. guttatus and M. decorus, as well as within M. decorus conform to the predictions of parental conflict: (1) reciprocal F1s exhibit size differences and parent-of-origin specific endosperm defects, (2) the extent of asymmetry between reciprocal F1 seed size is correlated with asymmetry in HSI, and (3) inferred differences in the extent of conflict predict the extent of HSI between populations. We also find that HSI is rapidly evolving, as populations that exhibit the most HSI are each others’ closest relative. Lastly, while all populations are largely outcrossing, we find that the differences in the inferred strength of conflict scale positively with π, suggesting that demographic or life history factors other than mating system may also influence the rate of parental conflict driven evolution. Overall, these patterns suggest the rapid evolution of parent-of-origin specific resource allocation alleles coincident with HSI within and between M. guttatus and M. decorus. Parental conflict may therefore be an important evolutionary driver of reproductive isolation.