Extreme changes to gene expression associated with homoploid hybrid speciation

Hybridization is an important cause of abrupt speciation. Hybrid speciation without a change in ploidy (homoploid hybrid speciation) is well-established in plants but has also been reported in animals and fungi. A notable example of recent homoploid hybrid speciation is Senecio squalidus (Oxford ragwort), which originated in the UK in the 18th Century following introduction of hybrid material from a hybrid zone between S. chrysanthemifolius and S. aethnensis on Mount Etna, Sicily. To investigate genetic divergence between these taxa, we used complementary DNA microarrays to compare patterns of floral gene expression. These analyses revealed major differences in gene expression between the parent species and wild and resynthesized S. squalidus . Comparisons of gene expression between S. aethnensis , S. chrysanthemifolius and natural S. squalidus identified genes potentially involved in local environmental adaptation. The analysis also revealed non-additive patterns of gene expression in the hybrid relative to its progenitors. These expression changes were more dramatic and widespread in resynthesized hybrids than in natural S. squalidus , suggesting that a unique expression pattern may have been fixed during the allopatric divergence of British S. squalidus . We speculate that hybridization-induced gene-expression change may provide an immediate source of novel phenotypic variation upon which selection can act to facilitate homoploid hybrid speciation in plants.     

Increasing evidence of the role of gene flow in animal evolution: hybrid speciation in the yellow-rumped warbler complex

In this issue of Molecular Ecology, Brelsford et al. (2011) present strong evidence for a case of hybrid speciation within the yellow-rumped warbler complex. Although homoploid hybrid speciation has now been documented in many animals (Mallet 2007), it seems rare in tetrapods (Mavárez & Linares 2008) and it has barely even been mentioned in birds (Price 2008). Brelsford and colleagues thus present the first detailed molecular evidence suggesting that hybrid speciation can occur in birds. Brelsford et al. (2011) posit that Audubon's warbler (Dendroica auduboni) constitutes a hybrid species originating from the admixture of two distinct parental lineages, represented today by myrtle warbler (D. coronata) and black-fronted warbler (D. nigrifrons). The authors present three major lines of molecular evidence suggesting that this is not simply a case of a hybrid swarm or limited introgression.     

Hybrid speciation in sparrows I: phenotypic intermediacy,genetic admixture and barriers to gene flow

Homoploid hybrid speciation is thought to require unusual circumstances to yield reproductive isolation from the parental species, and few examples are known from nature. Here, we present genetic evidence for this mode of speciation in birds. Using Bayesian assignment analyses of 751 individuals genotyped for 14 unlinked, nuclear microsatellite loci, we show that the phenotypically intermediate Italian sparrow (Passer italiae) does not form a cluster of its own, but instead exhibits clear admixture (over its entire breeding range) between its putative parental species, the house sparrow (P. domesticus) and the Spanish sparrow (P. hispaniolensis). Further, the Italian sparrow possesses mitochondrial (mt) DNA haplotypes identical to both putative parental species (although mostly of house sparrow type), indicating a recent hybrid origin. Today, the Italian sparrow has a largely allopatric distribution on the Italian peninsula and some Mediterranean islands separated from its suggested parental species by the Alps and the Mediterranean Sea, but co‐occurs with the Spanish sparrow on the Gargano peninsula in southeast Italy. No evidence of interbreeding was found in this sympatric population. However, the Italian sparrow hybridizes with the house sparrow in a sparsely populated contact zone in the Alps. Yet, the contact zone is characterized by steep clines in species‐specific male plumage traits, suggesting that partial reproductive isolation may also have developed between these two taxa. Thus, geographic and reproductive barriers restrict gene flow into the nascent hybrid species. We propose that an origin of hybrid species where the hybrid lineage gets geographically isolated from its parental species, as seems to have happened in this system, might be more common in nature than previously assumed.     

Behavioural isolation may facilitate homoploid hybrid speciation in cichlid fish

Hybrid speciation is constrained by the homogenizing effects of gene flow from the parental species. In the absence of post‐mating isolation due to structural changes in the genome, or temporal or spatial premating isolation, another form of reproductive isolation would be needed for homoploid hybrid speciation to occur. Here, we investigate the potential of behavioural mate choice to generate assortative mating among hybrids and parental species. We made three‐first‐generation hybrid crosses between different species of African cichlid fish. In three‐way mate‐choice experiments, we allowed hybrid and nonhybrid females to mate with either hybrid or nonhybrid males. We found that hybrids generally mated nonrandomly and that hybridization can lead to the expression of new combinations of traits and preferences that behaviourally isolate hybrids from both parental species. Specifically, we find that the phenotypic distinctiveness of hybrids predicts the symmetry and extent of their reproductive isolation. Our data suggest that behavioural mate choice among hybrids may facilitate the establishment of isolated hybrid populations, even in proximity to one or both parental species.     

Molecular genetic and quantitative trait divergence associated with recent homoploid hybrid speciation: a study of Senecio squalidus (Asteraceae)

Hybridization is increasingly seen as a trigger for rapid evolution and speciation. To quantify and qualify divergence associated with recent homoploid hybrid speciation, we compared quantitative trait (QT) and molecular genetic variation between the homoploid hybrid species Senecio squalidus and its parental species, S. aethnensis and S. chrysanthemifolius, and also their naturally occurring Sicilian hybrids. S. squalidus originated and became invasive in the United Kingdom following the introduction of hybrid plants from Mount Etna, Sicily, about 300 years ago. We recorded considerable molecular genetic differentiation between S. squalidus and its parents and their Sicilian hybrids in terms of both reduced genetic diversity and altered allele frequencies, potentially due to the genetic bottleneck associated with introduction to the United Kingdom. S. squalidus is also distinct from its parents and Sicilian hybrids for QTs, but less so than for molecular genetic markers. We suggest that this is due to resilience of polygenic QTs to changes in allele frequency or lack of selection for hybrid niche divergence in geographic isolation. While S. squalidus is intermediate or parental-like for most QTs, some trangressively distinct traits were observed, which might indicate emerging local adaptation in its invasive range. This study emphasizes the important contribution of founder events and geographic isolation to successful homoploid hybrid speciation.     

Major structural genomic alterations can be associated with hybrid speciation in Aegilops markgrafii (Triticeae)

During evolutionary history many grasses from the tribe Triticeae have undergone interspecific hybridization, resulting in allopolyploidy; whereas homoploid hybrid speciation was found only in rye. Homoeologous chromosomes within the Triticeae preserved cross‐species macrocolinearity, except for a few species with rearranged genomes. Aegilops markgrafii, a diploid wild relative of wheat (2n = 2x = 14), has a highly asymmetrical karyotype that is indicative of chromosome rearrangements. Molecular cytogenetics and next‐generation sequencing were used to explore the genome organization. Fluorescence in situ hybridization with a set of wheat cDNAs allowed the macrostructure and cross‐genome homoeology of the Ae. markgrafii chromosomes to be established. Two chromosomes maintained colinearity, whereas the remaining were highly rearranged as a result of inversions and inter‐ and intrachromosomal translocations. We used sets of barley and wheat orthologous gene sequences to compare discrete parts of the Ae. markgrafii genome involved in the rearrangements. Analysis of sequence identity profiles and phylogenic relationships grouped chromosome blocks into two distinct clusters. Chromosome painting revealed the distribution of transposable elements and differentiated chromosome blocks into two groups consistent with the sequence analyses. These data suggest that introgressive hybridization accompanied by gross chromosome rearrangements might have had an impact on karyotype evolution and homoploid speciation in Ae. markgrafii.     

Homoploid hybrid speciation in a rare endemic Castilleja from Idaho (Castilleja christii,Orobanchaceae)

• Premise of the study: Hybridization is an important evolutionary force in the history of angiosperms; however, there are few examples of stabilized species derived through homoploid hybrid speciation. Homoploid hybrid species are generally detected via the presence of genetic additivity of parental markers, novel ecological and spatial distinctions, and novel morphological traits, all of which may aid in the successful establishment of hybrid species from parental types. Speciation and diversification within the genus Castilleja (Orobanchaceae) has been attributed to high levels of hybridization and polyploidy, though currently there are no examples of homoploid hybrid speciation within the genus. We employed multiple lines of evidence to examine a putative hybrid origin in C. christii, a rare endemic, known only from 80 hectares at the summit of Mt. Harrison (Cassia Co., Idaho). • Methods: We used granule-bound starch synthase II (waxy) sequences and 26 morphological characters to address hybridization between C. christii and widespread congeners C. miniata and/or C. linariifolia in an area of sympatry. Chromosomes of C. christii were also counted for the first time. • Key results: All 230 direct-sequenced C. christii individuals had the additive genomes of both C. miniata and C. linariifolia. Castilleja christii shares traits with both parents but also has floral characters that are unique and transgressive. Cytological counts indicated that all three taxa are diploid. • Conclusions: We conclude that C. christii is a stabilized homoploid hybrid derivative of C. linariifolia and C. miniata and is likely following an independent evolutionary trajectory from its progenitors.     

Gene expression regulation and lineage evolution: the North and South tale of the hybrid polyploid Squalius alburnoides complex

The evolution of hybrid polyploid vertebrates, their viability and their perpetuation over evolutionary time have always been questions of great interest. However, little is known about the impact of hybridization and polyploidization on the regulatory networks that guarantee the appropriate quantitative and qualitative gene expression programme. The Squalius alburnoides complex of hybrid fish is an attractive system to address these questions, as it includes a wide variety of diploid and polyploid forms, and intricate systems of genetic exchange. Through the study of genome-specific allele expression of seven housekeeping and tissue-specific genes, we found that a gene copy silencing mechanism of dosage compensation exists throughout the distribution range of the complex. Here we show that the allele-specific patterns of silencing vary within the complex, according to the geographical origin and the type of genome involved in the hybridization process. In southern populations, triploids of S. alburnoides show an overall tendency for silencing the allele from the minority genome, while northern population polyploids exhibit preferential biallelic gene expression patterns, irrespective of genomic composition. The present findings further suggest that gene copy silencing and variable expression of specific allele combinations may be important processes in vertebrate polyploid evolution.     

Genetic divergence, range expansion and possible homoploid hybrid speciation among pine species in Northeast China

Although homoploid hybrid speciation in plants is probably more common than previously realized, there are few well-documented cases of homoploid hybrid origin in conifers. We examined genetic divergence between two currently widespread pines in Northeast China, Pinus sylvestris var. mongolica and Pinus densiflora, and also whether two narrowly distributed pines in the same region, Pinus funebris and Pinus takahasii, might have originated from the two widespread species by homoploid hybrid speciation. Our results, based on population genetic analysis of chloroplast (cp), mitochondrial (mt) DNA, and nuclear gene sequence variation, showed that the two widespread species were divergent for both cp- and mtDNA variation, and also for haplotype variation at two of eight nuclear gene loci surveyed. Our analysis further indicated that P. sylvestris var. mongolica and P. densiflora remained allopatric during the most severe Quaternary glacial period that occurred in Northeast China, but subsequently exhibited rapid range expansions. P. funebris and P. takahasii, were found to contain a mixture of chlorotypes and nuclear haplotypes that distinguish P. sylvestris var. mongolica and P. densiflora, in support of the hypothesis that they possibly originated via homoploid hybrid speciation following secondary contact and hybridization between P. sylvestris var. mongolica and P. densiflora.     

低拷贝核基因在异源多倍体植物中的进化与表达

异源多倍体植物在自然界中广泛分布。在这类植物谱系中, 低拷贝核基因具有特殊的进化特点和丰富的植物系统发生信息, 在转录水平存在基因沉默、基因激活和不均等表达等特点。以低拷贝核基因为主线, 概述了其在多倍体植物系统发生中的应用和相关注意事项, 并对其在多倍体植物中的表达变化及其分子机制进行了探讨, 系统地介绍了国际上相关领域的研究成果和最新动向。     

Recent, allopatric, homoploid hybrid speciation: the origin of Senecio squalidus (Asteraceae) in the British Isles from a hybrid zone on Mount Etna, Sicily

Homoploid hybrid speciation occurs through stabilization of a hybrid segregate (or segregates) isolated by premating and/or postmating barriers from parent taxa. Theory predicts that ecological and spatial isolation are of critical importance during homoploid hybrid speciation, and all confirmed homoploid hybrid species are ecologically isolated from their parents. Until recently, such species have been identified long after they originated, and consequently it has not been possible to determine the relative importance of spatial and ecological isolation during their origin. Here we present evidence for the recent origin (within the past 300 years) of a new homoploid hybrid species, Senecio squalidus (Asteraceae), in the British Isles, following long-distance dispersal of hybrid material from a hybrid zone between S. aethnensis and S. chrysanthemifolius on Mount Etna, Sicily, Italy. Historical records show that such hybrid material from Sicily was introduced to the Oxford Botanic Garden in Britain in the early part of the 18th century and that S. squalidus began to spread from there after approximately 90 years. A survey of randomly amplified polymorphic DNA/intersimple sequence repeats (RAPD/ISSR) marker variation demonstrated that S. squalidus is a diploid hybrid derivative of S. aethnensis and S. chrysanthemifolius that grow at high and low altitudes, respectively, on Mount Etna and that form a hybrid zone at intermediate altitudes. Senecio squalidus contained 11 of 13 RAPD/ISSR markers that were recorded at high frequency in S. chrysanthemifolius but were absent or occurred at low frequency in S. aethnensis, and 10 of 13 markers for which the reverse was true. Bayesian admixture analysis showed that all individuals of S. squalidus surveyed were of mixed ancestry with relatively high mean proportions of ancestry derived from both S. chrysanthemifolius and S. aethnensis (0.644 and 0.356, respectively). We argue that long-distance isolation of hybrid material from its parents on Mount Etna would have helped favor the origin and establishment of S. squalidus in the British Isles, regardless of whether the initial hybrid material introduced to Britain was preadapted to local conditions.     

Using differential introgression in hybrid zones to identify genomic regions involved in speciation

Hybrids between species provide information about the evolutionary processes involved in divergence. In addition to creating hybrids in the laboratory, biologists can take advantage of natural hybrid zones to understand the factors that shape gene flow between divergent lineages. In the early stages of speciation, most regions of the genome continue to flow freely between populations. Alternatively, the subset of the genome that confers reproductive barriers between nascent species is expected to reject introgression. Now enabled by advances in genomics, this perspective is motivating detailed comparisons of gene flow across genomic regions in hybrid zones. Here, I review methods for measuring and interpreting introgression at multiple loci in hybrid zones, focusing on the problem of identifying loci that contribute to reproductive isolation. Emerging patterns from multi-locus studies of hybrid zones are highlighted, including remarkable variance in introgression across the genome. Although existing methods have been useful, there is scope for development of new analytical approaches that better connect differential patterns of gene flow in hybrid zones with current knowledge of speciation mechanisms. I outline future prospects for differential introgression studies on a genomic scale.