scholarly journals Patterns of regulatory divergence and gene expression in hybrids are associated with molecular evolution in species undergoing gene flow

2021 ◽  
Author(s):  
Fernando Diaz ◽  
Jason Wolf ◽  
Reinaldo de Brito

The extent to which hybridization disrupts a gene's pattern of expression likely governs its propensity for introgression, while its extent of molecular divergence can itself underlie such disruption. Together, these phenomena shape the landscape of sequence and transcriptional divergence across the genome as species diverge. To understand this process, we examine gene expression inheritance, regulatory and molecular divergences in the reproductive transcriptomes of species linked by gene flow. The fruit flies Anastrepha fraterculus and A. obliqua show evidence of gene flow despite clear evolutionary divergence and incomplete reproductive isolation. We find that their transcriptional patterns are a mosaic between those typically observed within and between allopatric species. Genes showing transgressive expression in hybrids or cis-regulatory divergence between species are associated with greater molecular divergence. This may reflect pleiotropic constraints that make them more resistant to gene flow or they may be more likely to experience divergent selection. However, while these highly divergent genes are likely to be important contributors to species differences, they are relatively rare. Instead, most differentially regulated genes, including those linked to reproduction, show high degrees of dominance in hybrids and trans-regulated divergence between species, suggesting widespread genetic compatibility that allowed for the identified introgression. These findings provide insights into how postzygotic isolating mechanisms might evolve in the presence of gene flow: regions showing cis-regulatory divergence or transgressive expression contribute to reproductive isolation, while regions with dominant expression and trans-regulatory divergence act as a buffer of hybrid breakdown, facilitating introgression, and leading to a genomic mosaic of expression and sequence divergence.

1953 ◽  
Vol 85 (4) ◽  
pp. 141-151 ◽  
Author(s):  
Stanley G. Smith

According to Dobzhansky (1951a, p. 262) “Species are … groups of populations the gene exchange between which is limited or prevented by one, or by a combination of several, reproductive isolating mechanisms”. This definition follows from his concept of a species not as a static unit but as a stage in the process of evolutionary divergence. Limitation or prevention of gene exchange is a property of geographic and reproductive isolation (Mayr, 1912), the various types of which Dobzhansky lists as follows:I. Geographic or Spatial IsolationII. Reproductive IsolationA. Ecological IsolationB. Seasonal or Temporal IsolationC. Sexual, Psychological or Ethnological IsolationD. Mechanical IsolationE. Gametic IsolationF. Hybrid InviabilityG. Hybrid SterilityH. Hybrid Breakdown


Genome ◽  
2020 ◽  
pp. 1-11
Author(s):  
Bahar Patlar ◽  
Alberto Civetta

It has long been acknowledged that changes in the regulation of gene expression may account for major organismal differences. However, we still do not fully understand how changes in gene expression evolve and how do such changes influence organisms’ differences. We are even less aware of the impact such changes might have in restricting gene flow between species. Here, we focus on studies of gene expression and speciation in the Drosophila model. We review studies that have identified gene interactions in post-mating reproductive isolation and speciation, particularly those that modulate male gene expression. We also address studies that have experimentally manipulated changes in gene expression to test their effect in post-mating reproductive isolation. We highlight the need for a more in-depth analysis of the role of selection causing disrupted gene expression of such candidate genes in sterile/inviable hybrids. Moreover, we discuss the relevance to incorporate more routinely assays that simultaneously evaluate the potential effects of environmental factors and genetic background in modulating plastic responses in male genes and their potential role in speciation.


2019 ◽  
Vol 128 (3) ◽  
pp. 583-591
Author(s):  
Leo Joseph ◽  
Alex Drew ◽  
Ian J Mason ◽  
Jeffrey L Peters

Abstract We reassessed whether two parapatric non-sister Australian honeyeater species (Aves: Meliphagidae), varied and mangrove honeyeaters (Gavicalis versicolor and G. fasciogularis, respectively), that diverged from a common ancestor c. 2.5 Mya intergrade in the Townsville area of north-eastern Queensland. Consistent with a previous specimen-based study, by using genomics methods we show one-way gene flow for autosomal but not Z-linked markers from varied into mangrove honeyeaters. Introgression barely extends south of the area of parapatry in and around the city of Townsville. While demonstrating the long-term porosity of species boundaries over several million years, our data also suggest a clear role of sex chromosomes in maintaining reproductive isolation.


Heredity ◽  
2021 ◽  
Author(s):  
Yael S. Rodger ◽  
Alexandra Pavlova ◽  
Steve Sinclair ◽  
Melinda Pickup ◽  
Paul Sunnucks

AbstractConservation management can be aided by knowledge of genetic diversity and evolutionary history, so that ecological and evolutionary processes can be preserved. The Button Wrinklewort daisy (Rutidosis leptorrhynchoides) was a common component of grassy ecosystems in south-eastern Australia. It is now endangered due to extensive habitat loss and the impacts of livestock grazing, and is currently restricted to a few small populations in two regions >500 km apart, one in Victoria, the other in the Australian Capital Territory and nearby New South Wales (ACT/NSW). Using a genome-wide SNP dataset, we assessed patterns of genetic structure and genetic differentiation of 12 natural diploid populations. We estimated intrapopulation genetic diversity to scope sources for genetic management. Bayesian clustering and principal coordinate analyses showed strong population genetic differentiation between the two regions, and substantial substructure within ACT/NSW. A coalescent tree-building approach implemented in SNAPP indicated evolutionary divergence between the two distant regions. Among the populations screened, the last two known remaining Victorian populations had the highest genetic diversity, despite having among the lowest recent census sizes. A maximum likelihood population tree method implemented in TreeMix suggested little or no recent gene flow except potentially between very close neighbours. Populations that were more genetically distinctive had lower genetic diversity, suggesting that drift in isolation is likely driving population differentiation though loss of diversity, hence re-establishing gene flow among them is desirable. These results provide background knowledge for evidence-based conservation and support genetic rescue within and between regions to elevate genetic diversity and alleviate inbreeding.


2019 ◽  
Author(s):  
Joseph A. McGirr ◽  
Christopher H. Martin

AbstractEcological speciation occurs when reproductive isolation evolves as a byproduct of adaptive divergence between populations. However, it is unknown whether divergent ecological selection on gene regulation can directly cause reproductive isolation. Selection favoring regulatory divergence between species could result in gene misregulation in F1 hybrids and ultimately lower hybrid fitness. We combined 58 resequenced genomes with 124 transcriptomes to test this hypothesis in a young, sympatric radiation of Cyprinodon pupfishes endemic to San Salvador Island, Bahamas, which consists of a dietary generalist and two novel trophic specialists – a molluscivore and a scale-eater. We found more differential gene expression between closely related sympatric specialists than between allopatric generalist populations separated by 1000 km. Intriguingly, 9.6% of genes that were differentially expressed between sympatric species were also misregulated in their F1 hybrids. Consistent with divergent ecological selection causing misregulation, a subset of these genes were in highly differentiated genomic regions and enriched for functions important for trophic specialization, including head, muscle, and brain development. These regions also included genes that showed evidence of hard selective sweeps and were significantly associated with oral jaw length – the most rapidly diversifying skeletal trait in this radiation. Our results indicate that divergent ecological selection in sympatry can cause hybrid gene misregulation which may act as a primary reproductive barrier between nascent species.SignificanceIt is unknown whether the same genes that regulate ecological traits can simultaneously contribute to reproductive barriers between species. We measured gene expression in two trophic specialist species of Cyprinodon pupfishes that rapidly diverged from a generalist ancestor. We found genes differentially expressed between species that also showed extreme expression levels in their hybrid offspring. Many of these genes showed signs of selection and have putative effects on the development of traits that are important for ecological specialization. This suggests that genetic variants contributing to adaptive trait divergence between parental species negatively interact to cause hybrid gene misregulation, potentially producing unfit hybrids. Such loci may be important barriers to gene flow during the early stages of speciation, even in sympatry.


2014 ◽  
Author(s):  
Tiago Paixão ◽  
Kevin E. Bassler ◽  
Ricardo B. R. Azevedo

The Dobzhansky-Muller model posits that incompatibilities between alleles at different loci cause speciation. However, it is known that if the alleles involved in a Dobzhansky-Muller incompatibility (DMI) between two loci are neutral, the resulting reproductive isolation cannot be maintained in the presence of either mutation or gene flow. Here we show that speciation can emerge through the collective effects of multiple neutral DMIs that cannot, individually, cause speciation-a mechanism we call emergent speciation. We investigate emergent speciation using models of haploid holey adaptive landscapes-neutral networks-with recombination. We find that certain combinations of multiple neutral DMIs can lead to speciation. Furthermore, emergent speciation is a robust mechanism that can occur in the presence of migration, and of deviations from the assumptions of the neutral network model. Strong recombination and complex interactions between the DMI loci facilitate emergent speciation. These conditions are likely to occur in nature. We conclude that the interaction between DMIs may cause speciation.


2015 ◽  
Vol 112 (27) ◽  
pp. E3545-E3554 ◽  
Author(s):  
Xu Wang ◽  
John H. Werren ◽  
Andrew G. Clark

There is extraordinary diversity in sexual dimorphism (SD) among animals, but little is known about its epigenetic basis. To study the epigenetic architecture of SD in a haplodiploid system, we performed RNA-seq and whole-genome bisulfite sequencing of adult females and males from two closely related parasitoid wasps, Nasonia vitripennis and Nasonia giraulti. More than 75% of expressed genes displayed significantly sex-biased expression. As a consequence, expression profiles are more similar between species within each sex than between sexes within each species. Furthermore, extremely male- and female-biased genes are enriched for totally different functional categories: male-biased genes for key enzymes in sex-pheromone synthesis and female-biased genes for genes involved in epigenetic regulation of gene expression. Remarkably, just 70 highly expressed, extremely male-biased genes account for 10% of all transcripts in adult males. Unlike expression profiles, DNA methylomes are highly similar between sexes within species, with no consistent sex differences in methylation found. Therefore, methylation changes cannot explain the extensive level of sex-biased gene expression observed. Female-biased genes have smaller sequence divergence between species, higher conservation to other hymenopterans, and a broader expression range across development. Overall, female-biased genes have been recruited from genes with more conserved and broadly expressing “house-keeping” functions, whereas male-biased genes are more recently evolved and are predominately testis specific. In summary, Nasonia accomplish a striking degree of sex-biased expression without sex chromosomes or epigenetic differences in methylation. We propose that methylation provides a general signal for constitutive gene expression, whereas other sex-specific signals cause sex-biased gene expression.


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