The emerging importance of cross-ploidy hybridisation and introgression.

Natural hybridisation is now recognised as pervasive in its occurrence across the Tree of Life. Resurgent interest in natural hybridisation fuelled by developments in genomics has led to an improved understanding of the genetic factors that promote or prevent species cross-mating. Despite this body of work overturning many widely held assumptions about the genetic barriers to hybridisation, it is still widely thought that ploidy differences between species will be an absolute barrier to hybridisation and introgression. Here, we revisit this assumption, reviewing findings from surveys of polyploidy and hybridisation in the wild. In a case study in the British flora, 203 hybrids representing 35% of hybrids with suitable data have formed via cross-ploidy matings, while a wider literature search revealed 59 studies (56 in plants and 3 in animals) in which cross-ploidy hybridisation has been confirmed with genetic data. These results show cross-ploidy hybridisation is readily overlooked, and potentially common in some groups. General findings from these studies include strong directionality of hybridisation, with introgression usually towards the higher ploidy parent, and cross-ploidy hybridisation being more likely to involve allopolyploids than autopolyploids. Evidence for adaptive introgression across a ploidy barrier and cases of cross-ploidy hybrid speciation shows the potential for important evolutionary outcomes.

Abiotic Niche Divergence of Hybrid Species from Their Progenitors.

AbstractAlthough more frequently discussed recently than previously, the role of ecology in homoploid hybrid and allopolyploid speciation has not been subjected to comparative analysis. We examined abiotic niche divergence of 22 assumed homoploid hybrid species and 60 allopolyploid species from that of their progenitors. Ecological niche modeling was employed in an analysis of each species' fundamental niche, and ordination methods were used in an analysis of realized niches. Both analyses utilized 100,000 georeferenced records. From estimates of niche overlap and niche breadth, we identified for both types of hybrid species four niche divergence patterns: niche novelty, niche contraction, niche intermediacy, and niche expansion. Niche shifts involving niche novelty were common and considered likely to play an important role in the establishment of both types of hybrid species, although more so for homoploid hybrid species than for allopolyploid species. Approximately 70% of homoploid hybrid species versus 37% of allopolyploid species showed shifts in the fundamental niche from their parents, and ∼86% versus ∼52%, respectively, exhibited shifts in the realized niche. Climate was shown to contribute more than soil and landform to niche shifts in both types of hybrid species. Overall, our results highlight the significance of abiotic niche divergence for hybrid speciation, especially without genome duplication.

Ancient polymorphisms and divergence hitchhiking contribute to genomic islands of divergence within a poplar species complex.

How genome divergence eventually leads to speciation is a topic of prime evolutionary interest. Genomic islands of elevated divergence are frequently reported between diverging lineages, and their size is expected to increase with time and gene flow under the speciation-with-gene-flow model. However, such islands can also result from divergent sorting of ancient polymorphisms, recent ecological selection regardless of gene flow, and/or recurrent background selection and selective sweeps in low-recombination regions. It is challenging to disentangle these nonexclusive alternatives, but here we attempt to do this in an analysis of what drove genomic divergence between four lineages comprising a species complex of desert poplar trees. Within this complex we found that two morphologically delimited species, Populus euphratica and Populus pruinosa, were paraphyletic while the four lineages exhibited contrasting levels of gene flow and divergence times, providing a good system for testing hypotheses on the origin of divergence islands. We show that the size and number of genomic islands that distinguish lineages are not associated with either rate of recent gene flow or time of divergence. Instead, they are most likely derived from divergent sorting of ancient polymorphisms and divergence hitchhiking. We found that highly diverged genes under lineage-specific selection and putatively involved in ecological and morphological divergence occur both within and outside these islands. Our results highlight the need to incorporate demography, absolute divergence measurement, and gene flow rate to explain the formation of genomic islands and to identify potential genomic regions involved in speciation.

Senecio as a model system for integrating studies of genotype, phenotype and fitness.

Two major developments have made it possible to use examples of ecological radiations as model systems to understand evolution and ecology. First, the integration of quantitative genetics with ecological experiments allows detailed connections to be made between genotype, phenotype, and fitness in the field. Second, dramatic advances in molecular genetics have created new possibilities for integrating field and laboratory experiments with detailed genetic sequencing. Combining these approaches allows evolutionary biologists to better study the interplay between genotype, phenotype, and fitness to explore a wide range of evolutionary processes. Here, we present the genus Senecio (Asteraceae) as an excellent system to integrate these developments, and to address fundamental questions in ecology and evolution. Senecio is one of the largest and most phenotypically diverse genera of flowering plants, containing species ranging from woody perennials to herbaceous annuals. These Senecio species exhibit many growth habits, life histories, and morphologies, and they occupy a multitude of environments. Common within the genus are species that have hybridized naturally, undergone polyploidization, and colonized diverse environments, often through rapid phenotypic divergence and adaptive radiation. These diverse experimental attributes make Senecio an attractive model system in which to address a broad range of questions in evolution and ecology.

Population genomic analysis reveals that homoploid hybrid speciation can be a lengthy process.

An increasing number of species are thought to have originated by homoploid hybrid speciation (HHS), but in only a handful of cases are details of the process known. A previous study indicated that Picea purpurea, a conifer in the Qinghai-Tibet Plateau (QTP), originated through HHS from P. likiangensis and P. wilsonii. To investigate this origin in more detail, we analysed transcriptome data for 114 individuals collected from 34 populations of the three Picea species from their core distributions in the QTP. Phylogenetic, principal component and admixture analyses of nuclear SNPs showed the species to be delimited genetically and that P. purpurea was admixed with approximately 60% of its ancestry derived from P. wilsonii and 40% from P. likiangensis. Coalescent simulations revealed the best-fitting model of origin involved formation of an intermediate hybrid lineage between P. likiangensis and P. wilsonii approximately 6 million years ago (mya), which backcrossed to P. wilsonii to form P. purpurea approximately one mya. The intermediate hybrid lineage no longer exists and is referred to as a "ghost" lineage. Our study emphasizes the power of population genomic analysis combined with coalescent analysis for reconstructing the stages involved in the origin of a homoploid hybrid species over an extended period. In contrast to other studies, we show that these stages can in some instances span a relatively long period of evolutionary time.

Demographic expansion and genetic load of the halophyte model plant Eutrema salsugineum.

The halophyte model plant Eutrema salsugineum (Brassicaceae) disjunctly occurs in temperate to subarctic Asia and North America. This vast, yet extremely discontinuous distribution constitutes an ideal system to examine long-distance dispersal and the ensuing accumulation of deleterious mutations as expected in expanding populations of selfing plants. In this study, we resequenced individuals from 23 populations across the range of E. salsugineum. Our population genomic data indicate that E. salsugineum migrated "out of the Altai region" at least three times to colonize northern China, northeast Russia and western China. It then expanded its distribution into North America independently from northeast Russia and northern China, respectively. The species colonized northern China around 33.7 thousand years ago (kya) and underwent a considerable expansion in range size approximately 7-8 kya. The western China lineage is likely a hybrid derivative of the northern China and Altai lineages, originating approximately 25-30 kya. Deleterious alleles accumulated in a stepwise manner from (a) Altai to northern China and North America and (b) Altai to northeast Russia and North America. In summary, E. salsugineum dispersed from Asia to North America and deleterious mutations accumulated in a stepwise manner during the expansion of the species' distribution.

Chasing ghosts: allopolyploid origin of Oxyria sinensis (Polygonaceae) from its only diploid congener and an unknown ancestor.

Reconstructing the origin of a polyploid species is particularly challenging when an ancestor has become extinct. Under such circumstances, the extinct donor of a genome found in the polyploid may be treated as a 'ghost' species in that its prior existence is recognized through the presence of its genome in the polyploid. In this study, we aimed to determine the polyploid origin of Oxyria sinensis (2n = 40) for which only one congeneric species is known, that is diploid O. digyna (2n = 14). Genomic in situ hybridization (GISH), transcriptome, phylogenetic and demographic analyses, and ecological niche modelling were conducted for this purpose. GISH revealed that O. sinensis comprised 14 chromosomes from O. digyna and 26 chromosomes from an unknown ancestor. Transcriptome analysis indicated that following divergence from O. digyna, involving genome duplication around 12 million years ago (Ma), a second genome duplication occurred approximately 6 Ma to give rise to O. sinensis. Oxyria sinensis was shown to contain homologous gene sequences divergent from those present in O. digyna in addition to a set that clustered with those in O. digyna. Coalescent simulations indicated that O. sinensis expanded its distribution approximately 6-7 Ma, possibly following the second polyploidization event, whereas O. digyna expanded its range much later. It was also indicated that the distributions of both species contracted and re-expanded during the Pleistocene climatic oscillations. Ecological niche modelling similarly suggested that both species experienced changes in their distributional ranges in response to Quaternary climatic changes. The extinction of the unknown 'ghost' tetraploid species implicated in the origin of O. sinensis could have resulted from superior adaptation of O. sinensis to repeated climatic changes in the region where it now occurs.

Arctic plant origins and early formation of circumarctic distributions: a case study of the mountain sorrel, Oxyria digyna.

Many plant species comprising the present-day Arctic flora are thought to have originated in the high mountains of North America and Eurasia, migrated northwards as global temperatures fell during the late Tertiary period, and thereafter attained a circumarctic distribution. However, supporting evidence for this hypothesis that provides a temporal framework for the origin, spread and initial attainment of a circumarctic distribution by an arctic plant is currently lacking. Here we examined the origin and initial formation of a circumarctic distribution of the arctic mountain sorrel (Oxyria digyna) by conducting a phylogeographic analysis of plastid and nuclear gene DNA variation. We provide evidence for an origin of this species in the Qinghai-Tibet Plateau of southwestern China, followed by migration into Russia c. 11 million yr ago (Ma), eastwards into North America by c. 4 Ma, and westwards into Western Europe by c. 1.96 Ma. Thereafter, the species attained a circumarctic distribution by colonizing Greenland from both sides of the Atlantic Ocean. Following the arrival of the species in North America and Europe, population sizes appear to have increased and then stabilized there over the last 1 million yr. However, in Greenland a marked reduction followed by an expansion in population size is indicated to have occurred during the Pleistocene.

Morphological Convergence Between an Allopolyploid and One of its Parental Species Correlates with Biased Gene Expression and DNA Loss.

The contribution of gene expression modulation to phenotypic evolution is of major importance to an understanding of the origin of divergent or convergent phenotypes during and following polyploid speciation. Here, we analyzed genome-wide gene expression in 2 subspecies of the allotetraploid species, Senecio mohavensis A. Gray, and its diploid parents S. flavus (Decne.) Sch. Bip. and S. glaucus L. The tetraploid is morphologically much more similar to S. flavus, leading to earlier confusion over its taxonomic status. By means of an analysis of transcriptomes of all 3 species, we show that gene expression divergence between the parent species is relatively low (ca. 14% of loci), whereas there is significant unequal expression between ca. 20-25% of the parental homoeologues (gene copies) in the tetraploid. The majority of the expression bias in the tetraploid is in favor of S. flavus homoeologues (ca. 65% of the differentially expressed loci), and overall expression of this parental species subgenome is higher than that of the S. glaucus subgenome. To determine whether absence of expression of a particular S. glaucus homoeologue in the allotetraploid could be due to loss of DNA, we carried out a PCR-based assay and confirmed that in 3 out of 10 loci the S. glaucus homoeologue appeared absent. Our results suggest that biased gene expression is one cause of the allotetraploid S. mohavensis being more similar in morphology to one of its parent, S. flavus, and that such bias could result, in part, from loss of S. glaucus homoeologues at some loci in the allotetraploid.

Should I stay or should I go: biogeographic and evolutionary history of a polyploid complex (Chrysanthemum indicum complex) in response to Pleistocene climate change in China.

Quaternary climatic oscillations greatly influenced the distribution and pattern of biodiversity in the Northern Hemisphere. Here we examine how such oscillations in South East Asia may have affected the demographic and evolutionary history of a polyploid plant complex associated with semi-dry habitats. We analyzed plastid and nuclear ribosomal DNA (rDNA) internal transcribed spacer (ITS) sequence variation within the Chrysanthemum indicum complex (Asteraceae), which comprises diploid and polyploid plants distributed throughout China. In total, 368 individuals from 47 populations across the geographical range of the complex were analyzed. We show that the relatively widespread tetraploid form of C. indicum expanded its range southward in the Pleistocene, possibly during the most recent or previous glacial period when conditions became drier and forests retreated in southern China. In marked contrast, diploid and other polyploid members of the complex failed to expand their ranges at these times or have since undergone range contractions in contrast to tetraploid C. indicum. We conclude that hybridization and gene flow between taxa occurred frequently during the evolutionary history of the complex, causing considerable sharing of chlorotypes and ITS types. Nevertheless, taxa within ploidy levels could be largely distinguished according to chlorotype and/or ITS type.

Diploid hybrid origin of Ostryopsis intermedia (Betulaceae) in the Qinghai-Tibet Plateau triggered by Quaternary climate change.

Despite the well-known effects that Quaternary climate oscillations had on shaping intraspecific diversity, their role in driving homoploid hybrid speciation is less clear. Here, we examine their importance in the putative homoploid hybrid origin and evolution of Ostryopsis intermedia, a diploid species occurring in the Qinghai-Tibet Plateau (QTP), a biodiversity hotspot. We investigated interspecific relationships between this species and its only other congeners, O. davidiana and O. nobilis, based on four sets of nuclear and chloroplast population genetic data and tested alternative speciation hypotheses. All nuclear data distinguished the three species clearly and supported a close relationship between O. intermedia and the disjunctly distributed O. davidiana. Chloroplast DNA sequence variation identified two tentative lineages, which distinguished O. intermedia from O. davidiana; however, both were present in O. nobilis. Admixture analyses of genetic polymorphisms at 20 SSR loci and sequence variation at 11 nuclear loci and approximate Bayesian computation (ABC) tests supported the hypothesis that O. intermedia originated by homoploid hybrid speciation from O. davidiana and O. nobilis. We further estimated that O. davidiana and O. nobilis diverged 6-11 Ma, while O. intermedia originated 0.5-1.2 Ma when O. davidiana is believed to have migrated southward, contacted and hybridized with O. nobilis possibly during the largest Quaternary glaciation that occurred in this region. Our findings highlight the importance of Quaternary climate change in the QTP in causing hybrid speciation in this important biodiversity hotspot.

Evolutionary history of Purple cone spruce (Picea purpurea) in the Qinghai-Tibet Plateau: homoploid hybrid origin and Pleistocene expansion.

Hybridization and introgression can play an important role in speciation. Here, we examine their roles in the origin and evolution of Picea purpurea, a diploid spruce species occurring on the Qinghai-Tibet Plateau (QTP). Phylogenetic relationships and ecological differences between this species and its relatives, P. schrenkiana, P. likiangensis and P. wilsonii, are unclear. To clarify them, we surveyed sequence variation within and between them for 11 nuclear loci, three chloroplast (cp) and two mitochondrial (mt) DNA fragments, and examined their ecological requirements using ecological niche modelling. Initial analyses based on 11 nuclear loci rejected a close relationship between P. schrenkiana and P. purpurea. BP&P tests and ecological niche modelling indicated substantial divergence between the remaining three species and supported the species status of P. purpurea, which contained many private alleles as expected for a well-established species. Sequence variation for cpDNA and mtDNA suggested a close relationship between P. purpurea and P. wilsonii, while variation at the nuclear se1364 gene suggested P. purpurea was more closely related to P. likiangensis. Analyses of genetic divergence, Bayesian clustering and model comparison using approximate Bayesian computation (ABC) of nuclear (nr) DNA variation all supported the hypothesis that P. purpurea originated by homoploid hybrid speciation from P. wilsonii and P. likiangensis. The ABC analysis dated the origin of P. purpurea at the Pleistocene, and the estimated hybrid parameter indicated that 69% of its nuclear composition was contributed by P. likiangensis and 31% by P. wilsonii. Our results further suggested that during or immediately following its formation, P. purpurea was subject to organelle DNA introgression from P. wilsonii such that it came to possess both mtDNA and cpDNA of P. wilsonii. The estimated parameters indicated that following its origin, P. purpurea underwent an expansion during/after the largest Pleistocene glaciation recorded for the QTP.

Genomic changes and stabilization following homoploid hybrid speciation of the Oxford ragwort Senecio squalidus.

Oxford ragwort (Senecio squalidus) is one of only two homoploid hybrid species known to have originated very recently, so it is a unique model for determining genomic changes and stabilization following homoploid hybrid speciation. Here, we provide a chromosome-level genome assembly of S. squalidus with 95% of the assembly contained in the 10 longest scaffolds, corresponding to its haploid chromosome number. We annotated 30,249 protein-coding genes and estimated that ∼62% of the genome consists of repetitive elements. We then characterized genome-wide patterns of linkage disequilibrium, polymorphism, and divergence in S. squalidus and its two parental species, finding that (1) linkage disequilibrium is highly heterogeneous, with a region on chromosome 4 showing increased values across all three species but especially in S. squalidus; (2) regions harboring genetic incompatibilities between the two parental species tend to be large, show reduced recombination, and have lower polymorphism in S. squalidus; (3) the two parental species have an unequal contribution (70:30) to the genome of S. squalidus, with long blocks of parent-specific ancestry supporting a very rapid stabilization of the hybrid lineage after hybrid formation; and (4) genomic regions with major parent ancestry exhibit an overrepresentation of loci with evidence for divergent selection occurring between the two parental species on Mount Etna. Our results show that both genetic incompatibilities and natural selection play a role in determining genome-wide reorganization following hybrid speciation and that patterns associated with homoploid hybrid speciation-typically seen in much older systems-can evolve very quickly following hybridization.

Pleistocene climate change and the origin of two desert plant species, Pugionium cornutum and Pugionium dolabratum (Brassicaceae), in northwest China.

Pleistocene climate change has had an important effect in shaping intraspecific genetic variation in many species; however, its role in driving speciation is less clear. We examined the possibility of a Pleistocene origin of the only two representatives of the genus Pugionium (Brassicaceae), Pugionium cornutum and Pugionium dolabratum, which occupy different desert habitats in northwest China. We surveyed sequence variation for internal transcribed spacer (ITS), three chloroplast (cp) DNA fragments, and eight low-copy nuclear genes among individuals sampled from 11 populations of each species across their geographic ranges. One ITS mutation distinguished the two species, whereas mutations in cpDNA and the eight low-copy nuclear gene sequences were not species-specific. Although interspecific divergence varied greatly among nuclear gene sequences, in each case divergence was estimated to have occurred within the Pleistocene when deserts expanded in northwest China. Our findings point to the importance of Pleistocene climate change, in this case an increase in aridity, as a cause of speciation in Pugionium as a result of divergence in different habitats that formed in association with the expansion of deserts in China.

Pliocene intraspecific divergence and Plio-Pleistocene range expansions within Picea likiangensis (Lijiang spruce), a dominant forest tree of the Qinghai-Tibet Plateau.

A knowledge of intraspecific divergence and range dynamics of dominant forest trees in response to past geological and climate change is of major importance to an understanding of their recent evolution and demography. Such knowledge is informative of how forests were affected by environmental factors in the past and may provide pointers to their response to future environmental change. However, genetic signatures of such historical events are often weak at individual loci due to large effective population sizes and long generation times of forest trees. This problem can be overcome by analysing genetic variation across multiple loci. We used this approach to examine intraspecific divergence and past range dynamics in the conifer Picea likiangensis, a dominant tree of forests occurring in eastern and southern areas of the Qinghai-Tibet Plateau (QTP). We sequenced 13 nuclear loci, two mitochondrial DNA regions and three plastid (chloroplast) DNA regions in 177 individuals sampled from 22 natural populations of this species, and tested the hypothesis that its evolutionary history was markedly affected by Pliocene QTP uplifts and Quaternary climatic oscillations. Consistent with the taxonomic delimitation of the three morphologically divergent varieties examined, all individuals clustered into three genetic groups with intervariety admixture detected in regions of geographical overlap. Divergence between varieties was estimated to have occurred within the Pliocene and ecological niche modelling based on 20 ecological variables suggested that niche differentiation was high. Furthermore, modelling of population-genetic data indicated that two of the varieties (var. rubescens and var. linzhiensis) expanded their population sizes after the largest Quaternary glaciation in the QTP, while expansion of the third variety (var. likiangensis) began prior to this, probably following the Pliocene QTP uplift. These findings point to the importance of geological and climatic changes during the Pliocene and Pleistocene as causes of intraspecific diversification and range shifts of dominant tree species in the QTP biodiversity hot spot region.

Evolutionary origin of genomic structural variations in domestic yaks.

Yak has been subject to natural selection, human domestication and interspecific introgression during its evolution. However, genetic variants favored by each of these processes have not been distinguished previously. We constructed a graph-genome for 47 genomes of 7 cross-fertile bovine species. This allowed detection of 57,432 high-resolution structural variants (SVs) within and across the species, which were genotyped in 386 individuals. We distinguished the evolutionary origins of diverse SVs in domestic yaks by phylogenetic analyses. We further identified 334 genes overlapping with SVs in domestic yaks that bore potential signals of selection from wild yaks, plus an additional 686 genes introgressed from cattle. Nearly 90% of the domestic yaks were introgressed by cattle. Introgression of an SV spanning the KIT gene triggered the breeding of white domestic yaks. We validated a significant association of the selected stratified SVs with gene expression, which contributes to phenotypic variations. Our results highlight that SVs of different origins contribute to the phenotypic diversity of domestic yaks.

Out of the Qinghai-Tibet Plateau: evidence for the origin and dispersal of Eurasian temperate plants from a phylogeographic study of Hippophaë rhamnoides (Elaeagnaceae).

Numerous temperate plants now distributed across Eurasia are hypothesized to have originated and migrated from the Qinghai-Tibet Plateau (QTP) and adjacent regions. However, this hypothesis has never been tested through a phylogeographic analysis of a widely distributed species. Here, we use Hippophaë rhamnoides as a model to test this hypothesis. We collected 635 individuals from 63 populations of the nine subspecies of H. rhamnoides. We sequenced two maternally inherited chloroplast (cp) DNA fragments and also the bi-paternally inherited nuclear ribosomal ITS. We recovered five major clades in phylogenetic trees constructed from cpDNA and internal transcribed spacer (ITS) sequence variation. Most sampled individuals of six subspecies that are distributed in northern China, central Asia and Asia Minor/Europe, respectively, comprised monophyletic clades (or subclades) nested within those found in the QTP. Two subspecies in the QTP were paraphyletic, while the placement of another subspecies from the Mongolian Plateau differed between the ITS and cpDNA phylogenetic trees. Our phylogeographic analyses supported an 'out-of-QTP' hypothesis for H. rhamnoides followed by allopatric divergence, hybridization and introgression. These findings highlight the complexity of intraspecific evolutions and the importance of the QTP as a center of origin for many temperate plants.

Tales of the unexpected: phylogeography of the arctic-alpine model plant Saxifraga oppositifolia (Saxifragaceae) revisited.

Arctic-alpine biota occupy enormous areas in the Arctic and the northern hemisphere mountain ranges and have undergone major range shifts during their comparatively short history. The origins of individual arctic-alpine species remain largely unknown. In the case of the Purple saxifrage, Saxifraga oppositifolia, an important model for arctic-alpine plants, phylogeographic studies have remained inconclusive about early stages of the species' spatiotemporal diversification but have provided evidence for long-range colonization out of a presumed Beringian origin to cover today's circumpolar range. We re-evaluated the species' large-scale range dynamics based on a geographically extended sampling including crucial areas such as Central Asia and the (south-)eastern European mountain ranges and employing up-to-date phylogeographic analyses of a plastid sequence data set and a more restricted AFLP data set. In accordance with previous studies, we detected two major plastid DNA lineages also reflected in AFLP divergence, suggesting a long and independent vicariant history. Although we were unable to determine the species' area of origin, our results point to Europe (probably the Alps) and Central Asia, respectively, as the likely ancestral areas of the two main lineages. AFLP data suggested that contact areas between the two clades in the Carpathians, Northern Siberia and western Greenland were secondary. In marked contrast to high levels of diversity revealed in previous studies, populations from the major arctic refugium Beringia did not exhibit any plastid sequence polymorphism. Our study shows that adequate sampling of the southern, refugial populations is crucial for understanding the range dynamics of arctic-alpine species.

The genetic ghost of an invasion past: colonization and extinction revealed by historical hybridization in Senecio.

Hybridization is an important evolutionary factor in the diversification of many plant and animal species. Of particular interest is that historical hybridization resulting in the origin of new species or introgressants has occurred between species now geographically separated by great distances. Here, we report that Senecio massaicus, a tetraploid species native to Morocco and the Canary Islands, contains genetic material of two distinct, geographically separated lineages: a Mediterranean lineage and a mainly southern African lineage. A time-calibrated internal transcribed spacer phylogeny indicates that the hybridization event took place up to 6.18 Ma. Because the southern African lineage has never been recorded from Morocco or the Canary Islands, we hypothesize that it reached this area in the distant past, but never became permanently established. Interestingly, the southern African lineage includes S. inaequidens, a highly invasive species that has recently become widespread throughout Europe and was introduced at the end of the 19th century as a 'wool alien'. Our results suggest that this more recent invasion of Europe by S. inaequidens represents the second arrival of this lineage into the region.