Speciation genes in plants

Background

Analyses of speciation genes – genes that contribute to the cessation of gene flow between populations – can offer clues regarding the ecological settings, evolutionary forces and molecular mechanisms that drive the divergence of populations and species. This review discusses the identities and attributes of genes that contribute to reproductive isolation (RI) in plants, compares them with animal speciation genes and investigates what these genes can tell us about speciation.

Scope

Forty-one candidate speciation genes were identified in the plant literature. Of these, seven contributed to pre-pollination RI, one to post-pollination, prezygotic RI, eight to hybrid inviability, and 25 to hybrid sterility. Genes, gene families and genetic pathways that were frequently found to underlie the evolution of RI in different plant groups include the anthocyanin pathway and its regulators (pollinator isolation), S RNase-SI genes (unilateral incompatibility), disease resistance genes (hybrid necrosis), chimeric mitochondrial genes (cytoplasmic male sterility), and pentatricopeptide repeat family genes (cytoplasmic male sterility).

Conclusions

The most surprising conclusion from this review is that identities of genes underlying both prezygotic and postzygotic RI are often predictable in a broad sense from the phenotype of the reproductive barrier. Regulatory changes (both cis and trans) dominate the evolution of pre-pollination RI in plants, whereas a mix of regulatory mutations and changes in protein-coding genes underlie intrinsic postzygotic barriers. Also, loss-of-function mutations and copy number variation frequently contribute to RI. Although direct evidence of positive selection on speciation genes is surprisingly scarce in plants, analyses of gene family evolution, along with theoretical considerations, imply an important role for diversifying selection and genetic conflict in the evolution of RI. Unlike in animals, however, most candidate speciation genes in plants exhibit intraspecific polymorphism, consistent with an important role for stochastic forces and/or balancing selection in development of RI in plants.Key words: Speciation, reproductive isolation, mating system isolation, pollinator isolation, ecological isolation, unilateral incompatibility, hybrid necrosis, hybrid sterility, hybrid inviability, hybrid breakdown, cytoplasmic male sterility, restoration     

Genetic Architecture Underlying Nascent Speciation—The Evolution of Eurasian Pigs under Domestication

Speciation is a process whereby the evolution of reproductive barriers leads to isolated species. Although many studies have addressed large-effect genetic footprints in the advanced stages of speciation, the genetics of reproductive isolation in nascent stage of speciation remains unclear. Here, we show that pig domestication offers an interesting model for studying the early stages of speciation in great details. Pig breeds have not evolved the large X-effect of hybrid incompatibility commonly observed between “good species.” Instead, deleterious epistatic interactions among multiple autosomal loci are common. These weak Dobzhansky–Muller incompatibilities confer partial hybrid inviability with sex biases in crosses between European and East Asian domestic pigs. The genomic incompatibility is enriched in pathways for angiogenesis, androgen receptor signaling and immunity, with an observation of many highly differentiated cis-regulatory variants. Our study suggests that partial hybrid inviability caused by pervasive but weak interactions among autosomal loci may be a hallmark of nascent speciation in mammals.     

Cytonuclear incompatibility contributes to the early stages of speciation

Genetic incompatibility is a hallmark of speciation. Cytonuclear incompatibilities are proposed to be among the first genetic barriers to arise during speciation. Accordingly, reproductive isolation (RI) within species should be heavily influenced by interactions between the organelle and nuclear genomes. However, there are few clear examples of cytonuclear incompatibility within a species. Here, we show substantial postzygotic RI in first‐generation hybrids between differentiated populations of an herbaceous plant (up to 92% reduction in fitness). RI was primarily due to germination and survival, with moderate RI for pollen viability. RI for survival was asymmetric and caused by cytonuclear incompatibility, with the strength of incompatibility linearly related to chloroplast genetic distance. This cytonuclear incompatibility may be the result of a rapidly evolving plastid genome. Substantial asymmetric RI was also found for germination, but was not associated with cytonuclear incompatibility, indicating endosperm or maternal‐zygote incompatibilities. These results demonstrate that cytonuclear incompatibility contributes to RI within species, suggesting that initial rates of speciation could be influenced by rates of organelle evolution. However, other genetic incompatibilities are equally important, indicating that even at early stages, speciation can be a complex process involving multiple genes and incompatibilities.     

Signals of speciation within Arabidopsis thaliana in comparison with its relatives

The species within the now well-defined Arabidopsis genus provide biological materials suitable to investigate speciation and the development of reproductive isolation barriers between related species. Even within the model species A. thaliana, genetic differentiation between populations due to environmental adaptation or demographic history can lead to cases where hybrids between accessions are non-viable. Experimental evidence supports the importance of genome duplications and genetic epistatic interactions in the occurrence of reproductive isolation. Other examples of adaptation to specific environments can be found in Arabidopsis relatives where hybridization and chromosome doubling lead to new amphidiploid species. Molecular signals of speciation found in the Arabidopsis genus should provide a better understanding of speciation processes in plants from a genetic, molecular and evolutionary perspective.     

Persistent postmating,prezygotic reproductive isolation between populations

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.     

Extensive loss of Wnt genes in Tardigrada

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). 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. 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.     

Diverse paths to hybrid incompatibility in Arabidopsis

One of the most essential questions of biology is to understand how different species have evolved. Hybrid incompatibility, a phenomenon in which hybrids show reduced fitness in comparison with their parents, can result in reproductive isolation and speciation. Therefore, studying hybrid incompatibility provides an entry point in understanding speciation. Hybrid incompatibilities are known throughout taxa, and the underlying mechanisms have mystified scientists since the theory of evolution by means of natural selection was introduced. In plants, it is only in recent years that the high‐throughput genetic and molecular tools have become available for the Arabidopsis genus, thus helping to shed light on the different genes and molecular and evolutionary mechanisms that underlie hybrid incompatibilities. In this review, we highlight the current knowledge of diverse mechanisms that are known to contribute to hybrid incompatibility.     

GENETIC ARCHITECTURE AND POSTZYGOTIC REPRODUCTIVE ISOLATION: EVOLUTION OF BATESON–DOBZHANSKY–MULLER INCOMPATIBILITIES IN A POLYGENIC MODEL

The Bateson–Dobzhansky–Muller model predicts that postzygotic isolation evolves due to the accumulation of incompatible epistatic interactions, but few studies have quantified the relationship between genetic architecture and patterns of reproductive divergence. We examined how the direction and magnitude of epistatic interactions in a polygenic trait under stabilizing selection influenced the evolution of hybrid incompatibilities. We found that populations evolving independently under stabilizing selection experienced suites of compensatory allelic changes that resulted in genetic divergence between populations despite the maintenance of a stable, high‐fitness phenotype. A small number of loci were then incompatible with multiple alleles in the genetic background of the hybrid and the identity of these incompatibility loci changed over the evolution of the populations. For F₁ hybrids, reduced fitness evolved in a window of intermediate strengths of epistatic interactions, but F₂ and backcross hybrids evolved reduced fitness across weak and moderate strengths of epistasis due to segregation variance. Strong epistatic interactions constrained the allelic divergence of parental populations and prevented the development of reproductive isolation. Because many traits with varying genetic architectures must be under stabilizing selection, our results indicate that polygenetic drift is a plausible hypothesis for the evolution of postzygotic reproductive isolation.     

Evolution of reproductive isolation in plants

Reproductive isolation is essential for the process of speciation and much has been learned in recent years about the ecology and underlying genetics of reproductive barriers. But plant species are typically isolated not by a single factor, but by a large number of different pre- and postzygotic barriers, and their potentially complex interactions. This phenomenon has often been ignored to date. Recent studies of the relative importance of different isolating barriers between plant species pairs concluded that prezygotic isolation is much stronger than postzygotic isolation. But studies of the patterns of reproductive isolation in plants did not find that prezygotic isolation evolves faster than postzygotic isolation, in contrast to most animals. This may be due to the multiple premating barriers that isolate most species pairs, some of which may be controlled by few genes of major effect and evolve rapidly, whereas others have a complex genetic architecture and evolve more slowly. Intrinsic postzygotic isolation in plants is correlated with genetic divergence, but some instrinsic postzygotic barriers evolve rapidly and are polymorphic within species. Extrinsic postzygotic barriers are rarely included in estimates of different components of reproductive isolation. Much remains to be learned about ecological and molecular interactions among isolating barriers. The role of reinforcement and reproductive character displacement in the evolution of premating barriers is an open topic that deserves further study. At the molecular level, chromosomal and genic isolation factors may be associated and act in concert to mediate reproductive isolation, but their interactions are only starting to be explored.     

Differential patterns of introgression across the X chromosome in a hybrid zone between two species of house mice

A complete understanding of the speciation process requires the identification of genomic regions and genes that confer reproductive barriers between species. Empirical and theoretical research has revealed two important patterns in the evolution of reproductive isolation in animals: isolation typically arises as a result of disrupted epistatic interactions between multiple loci and these disruptions map disproportionately to the X chromosome. These patterns suggest that a targeted examination of natural gene flow between closely related species at X-linked markers with known positions would provide insight into the genetic basis of speciation. We take advantage of the existence of genomic data and a well-documented European zone of hybridization between two species of house mice, Mus domesticus and M. musculus, to conduct such a survey. We evaluate patterns of introgression across the hybrid zone for 13 diagnostic X-linked loci with known chromosomal positions using a maximum likelihood model. Interlocus comparisons clearly identify one locus with reduced introgression across the center of the hybrid zone, pinpointing a candidate region for reproductive isolation. Results also reveal one locus with high frequencies of M. domesticus alleles in populations on the M. musculus side of the zone, suggesting the possibility that positive selection may act to drive the spread of alleles from one species on to the genomic background of the other species. Finally, cline width and cline center are strongly positively correlated across the X chromosome, indicating that gene flow of the X chromosome may be asymmetrical. This study highlights the utility of natural populations of hybrids for mapping speciation genes and suggests that the middle of the X chromosome may be important for reproductive isolation between species of house mice.     

The effect of Wolbachia versus genetic incompatibilities on reinforcement and speciation

Wolbachia is a widespread group of intracellular bacteria commonly found in arthropods. In many insect species, Wolbachia induce a cytoplasmic mating incompatibility (CI). If different Wolbachia infections occur in the same host species, bidirectional CI is often induced. Bidirectional CI acts as a postzygotic isolation mechanism if parapatric host populations are infected with different Wolbachia strains. Therefore, it has been suggested that Wolbachia could promote speciation in their hosts. In this article we investigate theoretically whether Wolbachia-induced bidirectional CI selects for premating isolation and therefore reinforces genetic divergence between parapatric host populations. To achieve this we combined models for Wolbachia dynamics with a well-studied reinforcement model. This new model allows us to compare the effect of bidirectional CI on the evolution of female mating preferences with a situation in which postzygotic isolation is caused by nuclear genetic incompatibilities (NI). We distinguish between nuclear incompatibilities caused by two loci with epistatic interactions, and a single locus with incompatibility among heterozygotes in the diploid phase. Our main findings are: (1) bidirectional CI and single locus NI select for premating isolation with a higher speed and for a wider parameter range than epistatic NI; (2) under certain parameter values, runaway sexual selection leads to the increase of an introduced female preference allele and fixation of its preferred male trait allele in both populations, whereas under others it leads to divergence in the two populations in preference and trait alleles; and (3) bidirectional CI and single locus NI can stably persist up to migration rates that are two times higher than seen for epistatic NI. The latter finding is important because the speed with which mutants at the preference locus spread increases exponentially with the migration rate. In summary, our results show that bidirectional CI selects for rapid premating isolation and so generally support the view that Wolbachia can promote speciation in their hosts.     

The concept of effective recombination rate and its application in speciation theory

The goal of this study is to develop a unifying theoretical framework to quantify the strength of reproductive isolation. We propose the use of the "effective recombination rate," which measures how fast associations of genes are broken by interlocus recombination. Applying the well-established theory of the effective migration rate, we derive two techniques to investigate the effective recombination rate in models of speciation: the weak migration approximation for parapatric scenarios and the weak recombination approximation for sympatric scenarios. We illustrate the use of these two methods by two examples each: (1) single-locus genetic incompatibility and (2) two-locus genetic incompatibility for the first method, and (3) assortative mating and (4) assortative mating combined with disruptive selection for the second method. An advantage of the effective recombination rate over previous approaches is that it integrates gene flow in both directions into a single index measuring the strength of isolation. This enables straightforward comparisons of speciation scenarios with the same or different geographic histories. The method also allows us to evaluate the relative contributions of F2 hybrid deficiency or linkage between multiple barriers in reproductive isolation.     

ARE SPECIES REAL? THE SHAPE OF THE SPECIES BOUNDARY WITH EXPONENTIAL FAILURE,REINFORCEMENT, AND THE “MISSING SNOWBALL”

Under simple assumptions, the evolution of epistatic "Dobzhansky–Muller" incompatibilities between a pair of species should yield an accelerating decline of log overall reproductive compatibility—a "snowball" effect that might rapidly provide new species with "reality." Possible alternatives include: (1) simple exponential failure, giving a linear rate of log compatibility loss, and (2) "slowdown," likely during reinforcement in which mate choice evolves to prevent deleterious hybridization, yielding a decelerating log compatibility loss. In analyses of multiple datasets, we find little support for the snowball effect, except possibly in Lepidoptera hybrid viability. The snowball predicts a slow initial rate of incompatibility acquisition, with low initial variance; instead, highly variable compatibility is almost universally observed at low genetic distances. Another deviation from predictions is that reproductive isolation usually remains incomplete until long after speciation. These results do not disprove snowball compatibility decay, but can result if large deleterious effects are due to relatively few genetic changes, or if different types of incompatibility evolve at very different rates. On the other hand, data on Bacillus and Saccharomyces , as well as theories of chromosomal evolution, suggest that some kinds of incompatibility accumulate approximately linearly, without Dobzhansky–Muller effects. In microorganisms, linearity can result from direct negative effects of DNA sequence divergence on compatibility. Finally, a decelerating slowdown model is supported for sympatric Leptasterias starfish, and in Drosophila prezygotic isolation in sympatry but not allopatry, providing novel comparative evidence for reinforcement.     

植物物种形成的模式与机制

物种形成是指由已有的物种通过各种进化机制进化出新物种的过程。持续不断的物种形成产生了地球上灿烂的生物物种多样性。然而,研究人员对物种形成的模式与机制的了解却非常有限。一直以来,谱系分裂被认为是最重要的物种形成模式,但在植物中,谱系融合,即通过杂交形成新物种的过程,也是一个非常重要的物种形成模式。经过几十年的研究才逐渐认识到,生殖隔离是差异适应和遗传漂变的副产品,而不是物种形成的前提。相比合子形成后隔离,合子形成前的隔离在物种形成过程中更早地发挥作用。合子形成前的隔离,尤其是生态地理的隔离是植物中最重要的隔离机制。一些基于QTLs分析的研究发现,基因组中的少数主效位点在物种形成中起了关键作用,并且这些位点往往受到自然选择的作用。适应性辐射往往发生在隆起的山脉和新形成的岛屿上,很可能与这些地方能够提供很多可利用的生态位有关。最新的物种形成理论认为,基因是物种形成的基本单位,不同的物种可以在非控制物种差异适应性状的位点上存在基因流。这一观点为植物物种形成的研究提供了新的思路。随着植物物种形成研究的深入,越来越多植物物种形成基因被分离,包括花色素苷合成通路和S-基因座上的一些关键基因,揭示了植物物种形成的分子机制。前期的研究主要集中在模式植物和农作物上,许多生态上非常有趣的非模式植物还未得到广泛的研究。在未来的研究中,还需要更多来自非模式植物的例子以全面理解植物物种形成的多样化机制。     

Finding Hybrid Incompatibilities Using Genome Sequences from Hybrid Populations

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.     

Behavioural reproductive isolation and speciation in Drosophila

The origin of premating reproductive isolation continues to help elucidate the process of speciation and is the central event in the evolution of biological species. Therefore, during the process of species formation the diverging populations must acquire some means of reproductive isolation so that the genes from one gene pool are prevented from dispersing freely into a foreign gene pool. In the genus Drosophila, the phenomenon of behavioural reproductive isolation, which is an important type of premating (prezygotic) reproductive isolating mechanisms, has been extensively studied and interesting data have been documented. In many cases incomplete sexual isolation has been observed and the pattern and degree of isolation within and between the species have often been used to elucidate the phylogenetic relationships. The present review documents an overview of speciation mediated through behavioural incompatibility in different species groups of Drosophila with particular reference to the models proposed on the basis of one-sided ethological isolation to predict the direction of evolution. This study is crucial for understanding the mechanism of speciation through behavioural incompatibility and also for an understanding of speciation genetics in future prospects.     

Deleterious epistatic interactions between electron transport system protein-coding loci in the copepod Tigriopus californicus

The nature of epistatic interactions between genes encoding interacting proteins in hybrid organisms can have important implications for the evolution of postzygotic reproductive isolation and speciation. At this point very little is known about the fitness differences caused by specific closely interacting but evolutionarily divergent proteins in hybrids between populations or species. The intertidal copepod Tigriopus californicus provides an excellent model in which to study such interactions because the species range includes numerous genetically divergent populations that are still capable of being crossed in the laboratory. Here, the effect on fitness due to the interactions of three complex III proteins of the electron transport system in F2 hybrid copepods resulting from crosses of a pair of divergent populations is examined. Significant deviations from Mendelian inheritance are observed for each of the three genes in F2 hybrid adults but not in nauplii (larvae). The two-way interactions between these genes also have a significant impact upon the viability of these hybrid copepods. Dominance appears to play an important role in mediating the interactions between these loci as deviations are caused by heterozygote/homozygote deleterious interactions. These results suggest that the fitness consequences of the interactions of these three complex III-associated genes could influence reproductive isolation in this system.     

Sexual isolation and speciation in bacteria

Like organisms from all other walks of life, bacteria are capable of sexual recombination. However, unlike most plants and animals, bacteria recombine only rarely, and when they do they are extremely promiscuous in their choice of sexual partners. There may be no absolute constraints on the evolutionary distances that can be traversed through recombination in the bacterial world, but interspecies recombination is reduced by a variety of factors, including ecological isolation, behavioral isolation, obstacles to DNA entry, restriction endonuclease activity, resistance to integration of divergent DNA sequences, reversal of recombination by mismatch repair, and functional incompatibility of recombined segments. Typically, individual bacterial species are genetically variable for most of these factors. Therefore, natural selection can modulate levels of sexual isolation, to increase the transfer of genes useful to the recipient while minimizing the transfer of harmful genes. Interspecies recombination is optimized when recombination involves short segments that are just long enough to transfer an adaptation, without co-transferring potentially harmful DNA flanking the adaptation. Natural selection has apparently acted to reduce sexual isolation between bacterial species. Evolution of sexual isolation is not a milestone toward speciation in bacteria, since bacterial recombination is too rare to oppose adaptive divergence between incipient species. Ironically, recombination between incipient bacterial species may actually foster the speciation process, by prohibiting one incipient species from out-competing the other to extinction. Interspecific recombination may also foster speciation by introducing novel gene loci from divergent species, allowing invasion of new niches.     

SPECIATION DUE TO HYBRID NECROSIS IN PLANT–PATHOGEN MODELS

We develop a model for speciation due to postzygotic incompatibility generated by autoimmune reactions. The model is based on frequency‐dependent interactions between host plants and their pathogens, which can generate disruptive selection and give rise to speciation if distant phenotypes become reproductively isolated. Based on recent experimental evidence from Arabidopsis, we assume that at the molecular level, incompatibility between host strains is caused by epistatic interactions between two proteins in the plant immune system—the guard and the guardee. Within each plant strain, immune reactions occur when the guardee protein is modified by a pathogen effector, and the guard subsequently binds to the guardee, thus precipitating an immune response. When guard and guardee proteins come from phenotypically distant parents, a hybrid's immune system can be triggered by erroneous interactions between these proteins even in the absence of pathogen attack, leading to severe autoimmune reactions in hybrids. This generates a Dobzhnasky–Muller incompatibility due to immune reactions. Our model shows how phenotypic variation generated by frequency‐dependent host–pathogen interactions can lead to such postzygotic incompatibilities between extremal types, and hence to speciation.