Speciation, Chromosomal Rearrangements and

Speciation, Chromosomal Rearrangements and B Jackson, University of Sheffield, Sheffield, UK R Butlin, University of Sheffield, Sheffield, UK; and University of Gothenburg, Strömstad, Sweden A Navarro, Institute of Evolutionary Biology (Universitat Pompeu Fabra-CSIC), Barcelona, Catalonia, Spain; Centre de Regulació Genòmica (CRG), Barcelona, Catalonia, Spain; National Institute for Bioinformatics (INB), Barcelona, Catalonia, Spain; and Institució Catalana de Recerca i Estudis Avançats (ICREA), Catalonia, Spain R Faria, Institute of Evolutionary Biology (Universitat Pompeu Fabra-CSIC), Barcelona, Catalonia, Spain; and CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO, Laboratório Associado, Universidade do Porto, Vairão, Portugal r 2016 Elsevier Inc. All rights reserved.

Glossary Breakpoints Genomic regions delimiting chromosomal rearrangements. Collinear regions Chromosomal regions with the same gene order (i.e., without rearrangements). Dobzhansky–Muller incompatibilities (DMI) Epistatic interactions between alleles that manifest in hybrids by lowering their fitness. Epistatic effect Effect of an allele on a trait (or on fitness) that depends on its interactions with alleles at other loci (genetic background). Heterokaryotype Individual that is heterozygote for a chromosomal rearrangement. Meiotic drive Distortion in the expected transmission ratio (50:50) of a particular allele or chromosome at meiosis.

CRs Within and Between Natural Populations The history of evolutionary genetics is inextricably linked with the classic work on chromosomal rearrangements (CRs) in Drosophila by Alfred Sturtevant, Theodosius Dobzhansky and other early-twentieth century pioneers. In the 1910s and 1920s, a series of genetic factors were discovered in Drosophila that prevented recombination as heterozygotes, but did not have the same effect as homozygotes (e.g., Sturtevant, 1917, reviewed in Graubard, 1932). Sturtevant (1926) explained this phenomenon by showing that these recombination suppressors were chromosomal inversions segregating within Drosophila melanogaster (Sturtevant, 1921; Sturtevant and Plunkett, 1926; Sturtevant, 1926). Subsequently, population geneticists spent half a century investigating inversion polymorphisms within, and fixed inversion differences between, Drosophila species (Dobzhansky, 1970). Originally using the order of markers inferred from linkage maps, as in Sturtevant’s pioneering work, the process was greatly facilitated by the ease with which rearrangements can be characterized in Diptera using giant polytene chromosomes from larval salivary glands (Dobzhansky and Sturtevant, 1938; Dobzhansky, 1970). For some beautiful examples of how abnormal pairing in heterokaryotypes allowed the elucidation of inversion polymorphisms in Drosophila pseudoobscura see Dobzhansky and Sturtevant (1938) and Figure 1. These studies provided early examples of adaptive polymorphism segregating within species, with evidence that the frequency of

Encyclopedia of Evolutionary Biology, Volume 4

Post-zygotic barrier Contribution to reproductive isolation that operates after zygote formation, for example, hybrid sterility, hybrid inviability or ecologically dependent selection against hybrids. Pre-zygotic barrier Contribution to reproductive isolation that operates before zygote formation, for example, mate preference, habitat preference, temporal isolation, selection against immigrants, or gametic incompatibility. Reinforcement The evolution or strengthening of a prezygotic barrier between two populations as a consequence of natural selection against hybrids. Underdominance Case where the fitness of the heterozygote is lower than the fitness of either homozygote.

chromosomal inversions fluctuated cyclically and geographically in line with seasonal, altitudinal, and latitudinal climatic changes (Dobzhansky, 1943; Dobzhansky et al., 1966; Krimbas and Powell, 1992). They also introduced the ideas of supergenes (Dobzhansky and Pavlovsky, 1958; Prakash and Lewontin, 1968) and of position effects, where inversions might be adaptive by changing the relative positions of genes (reviewed in Dobzhansky, 1970). With the rise of modern genetics techniques, starting with allozymes in the 1960s, CRs were less frequently used as markers to study genetic variation, and this rich literature was largely forgotten (Kirkpatrick, 2010). In the genomic era, however, it seems that the importance of CRs has become apparent once more (Coghlan et al., 2005). Modern sequencing techniques have afforded even greater insight into the prevalence of CRs, by empowering researchers to detect fine-scale structural changes that could not be resolved cytogenetically (Alkan et al., 2011). It now seems clearer than ever that CRs are an important source of genetic variation and are widespread both within and between taxa, although this finding might not have surprised the classical Drosophila geneticists mentioned above. Genomic studies have shown that inversions are common and evolve rapidly in Drosophila, at a rate of around one new fixed inversion per million years (Ranz et al., 2001). The rate of chromosomal change may be even faster in nematodes, up to four times the rate in Drosophila (Coghlan and Wolfe, 2002). The comparison of genome sequences has revealed around 1500 inversion differences

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Figure 1 Representation of the pairing between homologous polytene chromosomes differing by a paracentric inversion in Drosophila pseudoobscura and possible consequences at meiosis. (a) Partial map of chromosome 3 (standard arrangement) showing several sections (scale in mm) and the location of the breakpoints (in red) of the ‘Arrowhead’ inversion, adapted from Dobzhansky, T., Sturtevant, A.H., 1938. Inversions in the chromosomes of Drosophila pseudoobscura. Genetics 23(1), 28–64 with permission from the Genetics Society of America; and schematic representation of part of the ‘Standard’ (black) and the ‘Arrowhead’ (white) chromosomes illustrating the reverse section order within the inversion. (b) Pairing of these homologous chromosomes in heterokaryotypes forming a loop structure (original representation reproduced from Dobzhansky, T., Sturtevant, A.H., 1938. Inversions in the chromosomes of Drosophila pseudoobscura. Genetics 23(1), 28–64) (left) and cartoon used in (c) (right). (c) Representation of three possible outcomes at meiosis after crossover(s) (green asterisk): C.1- one crossover in the collinear region resulting in full fertility/viability; C.2- one crossover within the inverted region generating unbalanced gametes (infertility/inviability); and C.3- double crossover (or gene conversion) within the inverted region resulting in viable gametes.

Speciation, Chromosomal Rearrangements and

between chimpanzees and humans (Feuk et al., 2005; Kirkpatrick, 2010). Despite many false positives (see also Chaisson et al., 2006), the number of true inversions is much higher than the nine discovered by classical cytogenetics (Yunis and Prakash, 1982). What’s more, when investigated further, many of these inversion differences were found to exist as polymorphisms within humans (Feuk et al., 2005). There is also evidence for extensive chromosomal variation within and between plant taxa. Levin (2000) reviewed examples of the prevalence in CRs in the genera Chaenactis, Clarkia, Coreopsis, Gaura, Gilia, Helianthus, and Lens, with a focus on their role in reproductive isolation. The recent access to whole genome sequences not only revealed a larger number of CRs but also a higher diversity of structural variants (including indels, copy-number variation, transposition, centromere repositioning) than previously considered (Rocchi et al., 2012; Rogers and Gibbs, 2014). Here we focus on large-scale rearrangements, fusions/fissions, translocations, and inversions that affect many genes, rather than on small scale or insertion/deletion changes. We do not consider changes in ploidy, which are the focus of another chapter.

The Establishment of CRs in Natural Populations If CRs are common in nature, how do they become established? Typically, newly arisen CRs show some level of underdominance and therefore should be eliminated from populations (details below, but see Dobzhansky, 1970). Because of this, rearrangements might be more easily established by drift in very small populations (e.g., Walsh, 1982; Lande, 1985; Spirito, 1998). The frequent demographic fluctuations experienced by annual plants together with self-fertilization, may explain why they tend to have a large number of CRs, since both traits reduce effective population size and selfing can generate homozygotes for rare variants, helping to overcome underdominance (Hoffmann and Rieseberg, 2008; Kirkpatrick, 2010). In species with large effective population sizes, other mechanisms are needed to explain the establishment of underdominant CRs. One possibility is meiotic drive (White, 1978, chap. 6), which may explain the fixation of any type of rearrangement, but particularly those involving Robertsonian fusions/fissions that alter centromere properties and so may cause biased segregation in females (Pardo-Manuel de Villena and Sapienza, 2001a; Pardo-Manuel de Villena and Sapienza, 2001b). Association between CRs and segregation distortion is also expected because suppressed recombination within the region encompassed by the chromosomal rearrangement (Figure 1) can benefit a driving system by establishing linkage between drivers and responders (McDermott and Noor, 2010). However, evidence for segregation distortion of rearrangements is mixed (e.g., Gropp and Winking, 1981; Britton-Davidian et al., 1990) and empirical studies of the association between segregation distortion and hybrid sterility have been limited largely to Drosophila (McDermott and Noor, 2010). Other forms of selection may also favor the establishment of CRs. Mayr (1945) first articulated the idea that rearrangements could be adaptive to certain habitats (White, 1978). This might be through direct effects: a rearrangement’s breakpoints may

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cause alterations in the open reading frames of genes or changes in gene expression due to promoter disruption or alteration of the relative positions of genes and regulatory regions (reviewed by Dobzhansky, 1970; Pérez-Ortín et al., 2002; Avelar et al., 2013). Alternatively, Dobzhansky suggested that inversions might hold together ‘coadapted complexes of genes’ (Dobzhansky, 1950; Wasserman, 1968), which can be interpreted as pairs or groups of loci with epistatic effects on fitness. Charlesworth and Charlesworth (1973) showed that the suppression of recombination by a newly arisen inversion could cause it to spread if it binds together an already-segregating combination of alleles presenting favorable epistatic interactions. A recent model (Kirkpatrick and Barton, 2006) shows how a CR can spread due to geographically divergent selection with gene flow, even in the absence of epistasis and when the CR itself has a small fitness cost. A new CR can become established if it traps advantageous alleles at two or more adaptive loci and if there is gene flow introducing locally maladaptive alleles at those loci. The inversion prevents the formation of suboptimal haplotypes (Figure 1), tying the locally adapted alleles together. This model can also explain why some inversions present a clinal distribution across environmental gradients, for example, in mosquitoes of the genus Anopheles (Costantini et al., 2009; Ayala et al., 2014) and in Drosophila (Krimbas and Powell, 1992; Hoffmann and Rieseberg, 2008). The Kirkpatrick and Barton process may not be powerful enough to increase the frequency of rearrangements when they first appear as single copy in one heterokaryotypic individual (Feder et al., 2011). Furthermore, the fixation of strongly underdominant CRs implies that several loci involved in adaptation must be captured in the same chromosomal region (Stathos and Fishman, 2014). This may be an unrealistic requirement for many systems. Feder et al. (2011) proposed a ‘mixed geographic model’ that relaxes these conditions: inversions can more easily become fixed during an alternating cycle of geographic isolation and gene flow. In an initial period of allopatry between two locally adapted populations, an inversion slightly increases in frequency due to drift; in a subsequent secondary contact the inversion spreads by the mechanism suggested by Kirkpatrick and Barton’s model, because it carries alleles involved in local adaptation, to an equilibrium frequency maintained by selection and migration. In a new phase of allopatry, the inversion may end up being fixed.

Early Models for the Role of CRs in Speciation The perceived importance of CRs in speciation peaked with the publication of M. J. D. White’s book, Modes of Speciation (White, 1978) and was still being championed much later than this (King, 1993). Motivated by the frequent observation of chromosomal differences among closely related species and the observation that in some taxa speciation rates are significantly correlated with the rate of chromosomal evolution (Levin and Wilson, 1976; Bush et al., 1977), White concluded that “it appears as if such [chromosomal] rearrangements, of many different types, have played the primary role in the majority of speciation events” (White, 1978, p. 336).

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White was a major proponent of a class of ‘chromosomal speciation’ model whose general mechanism involves negative fitness effects in heterokaryotypes and can be summarized as follows: CRs that differ between populations generate intrinsic post-zygotic barriers to gene flow because heterokaryotes experience mechanical problems with chromosomes (misspairing and nondisjunction) at meiosis and/or their gametes suffer insertions or deletions (i.e., are unbalanced) (Figure 1; White, 1978; Davisson and Akeson, 1993). Thus rearrangements are strongly underdominant. White (1978, p. 55) cited the example of Mus musculus (house mouse; 2n¼ 40), which differs from Mus poschiavinus (tobacco mouse; 2n¼ 26) by multiple chromosome fusions: nondisjunction in meiosis occurs at a rate of 6–33%, strongly reducing hybrid fecundity. Variants of these chromosomal speciation models (also called ‘hybrid-dysfunction’ models (Ayala and Coluzzi, 2005)) which date from between the 1960s and 1980s, are described by Rieseberg (2001). Most of them suffer from the same problem: in order to be strong barriers to gene flow, CRs must be strongly underdominant. But strongly underdominant rearrangements are unlikely to fix in natural populations because when they first arise they do so as heterokaryotypes, which are selected against (Spirito, 1998). An exception is the case where single rearrangements have very small effects on fitness but interactions between different rearrangements can have large effects: a chromosomal equivalent of the standard Dobzhansky–Muller model for intrinsic incompatibility (i.e., Dobzhansky–Muller incompatibilities – DMIs (Orr, 1995)). For example, the common shrew (Sorex araneus), exists as multiple chromosome races over its Palearctic range, each race having a different combination of fusions from an ancestral acrocentric karyotype. A single fusion has little effect on hybrid fertility but a pair of fusions can be highly incompatible (such as a ko fusion in one race and a bk fusion in another, described as ‘monobrachial homology’) (Searle, 1993). At the center of a hybrid zone between two races, shrews with acrocentric chromosomes ‘reappear,’ apparently favored by selection against the mismatched metacentric combinations (Searle, 1993). The difficulty of fixing underdominant rearrangements means that these historic models for the role of CRs in speciation often rely on some sort of geographic isolation during the speciation process (Rieseberg, 2001). There are also problems with their generality. Because crossovers are suppressed within some CRs, no unbalanced gametes are produced at meiosis, which challenges the idea that CRs always reduce fertility (Coyne et al., 1991, 1993). Hybrid inviability is at least as common as hybrid sterility as a barrier to gene flow, but heterozygosity for CRs is expected to cause the latter much more frequently. These and other patterns (Rieseberg, 2001; Coyne and Orr, 2004, pp. 259–260), suggest that genic factors are at least as important as chromosomal factors in generating incompatibilities. These problems ultimately led to hybrid-dysfunction models falling out of favor amongst most speciation biologists.

A New Role for CRs in Speciation Interest in the role of CRs in speciation was rekindled by the simultaneous publication, in 2001, of works by Rieseberg (2001) and Noor et al. (2001). These authors hit upon the idea

that the recombination reducing effect of CRs might facilitate speciation without reducing hybrid fitness (Figure 2). In fact, recombination-suppression models predate Rieseberg and Noor et al.’s work: see, for example, Dobzhansky (1950) who suggested that balanced inversion polymorphisms within populations maintained coadapted gene complexes, whilst heterokaryotypes for inversions derived from different populations were less fit; Coluzzi (1982) who suggested that inversions might maintain favorable (adapted) gene associations in novel ecological conditions; and Trickett and Butlin (1994) who showed that the recombination-suppression properties of CRs increased the likelihood of speciation in some older models (Felsenstein, 1981; Kirkpatrick, 1982). Rieseberg (2001) was inspired by his work in sunflowers (Helianthus spp.) from which he suggested that isolation genes within CRs might prevent gene flow across larger regions of the genome than isolation genes alone. Noor et al. (2001) were likewise inspired by their own results, in Drosophila, and suggested that CRs might delay the fusion of incipient species following secondary contact, by maintaining DMIs that would be lost from collinear regions due to recombination. Although their ideas are not mutually exclusive, Rieseberg (2001) put the emphasis on the role of CRs in accumulating the fitness effects of different isolation loci, due to suppressed recombination, and thus preventing gene flow across a larger fraction of the genome (Ortíz-Barrientos et al., 2002). In contrast, Noor et al. (2001) focused on the asymmetric nature of incompatibilities, which would explain why they would be lost in collinear regions but maintained in CRs (Ortíz-Barrientos et al., 2002). Noor et al. (2001) noted that, in their model, CRs increase the opportunity for the evolution of further pre-zygotic barriers between hybridizing taxa, i.e., reinforcement, but this is actually a general feature of chromosomal speciation models (Figure 2). Rieseberg and Noor et al.’s models were followed by further theoretical developments. Navarro and Barton (2003a) showed that DMIs are more likely to accumulate if CRs reduce recombination. Under a scenario of divergence with gene flow, their simulations showed that CRs can act as barriers by delaying the fixation of universally advantageous alleles, allowing the establishment and accumulation of incompatibilities. Together, these three models reconciled previously distinct ‘genic’ and ‘chromosomal’ views of speciation, by showing that both processes can work together in establishing reproductive isolation. Although none of these models addressed the initial requirement for a CR to become established in a natural population in the presence of gene flow, this problem has been solved in a rather general way by the Kirkpatrick and Barton (2006) model described above (and see Kirkpatrick, 2010, for further generalization). Kirkpatrick and Barton’s (2006) mechanism begins with local adaptation, resulting in some reproductive isolation. This is enhanced by the spread of the CR. The resulting chromosomal difference between demes may then facilitate speciation by the accumulation of further incompatibilities, further adaptive divergence, or reinforcement. Taken together, these recombination-suppression models suggest that multiple classes of reproductive barriers, both pre- and post-zygotic, can be associated with CRs if they are involved in speciation and some of the empirical examples we discuss below support this prediction. The chronology of the

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Continuum Isolation between demes

Independent evolution of CR and genic differences in both demes Reproductive isolation evolves (genic or CR DMIs) plus LA

1. Resumption of gene flow allows increase in frequency of CRs (MGM)

Gene flow between demes

Establishment of underdominant CRs by drive, selection (White)

LA and origin of CRs which capture adapted alleles

Possible establishment of underdominant CRs, by drift, drive, selection

2. Subsequent re-isolation can promote fixation of CRs (MGM)

Secondary contact

Loss of differences outside CRs. DMIs within CRs are retained and CRs play a interact (Noor) ‘protective’ role (Rieseberg)

Newly arisen CRs spread potentially to fixation (K&B)

RI due to CRs, LA

Accumulation of differences (including DMIs): by N&B, further LA, reinforcement. CRs play a ‘protective’ role (Rieseberg) Even less gene flow, potentially due to ‘snowballing’ accumulation of DMIs (N&B)

Progress toward complete RI Figure 2 A schematic representation of some different paths toward reproductive isolation (RI) between two demes, invoking different processes that involve chromosomal rearrangements (CRs). We illustrate two starting points: the presence and absence of gene flow (blue arrows) between the demes, representing ends of a continuum. Different deme colors represent the accumulation of (genic or CR) differences from the ancestral (blue) condition: the accumulation of incompatibilities is represented by progress toward darker red in one of the two demes. A double dagger represents the situation where chromosomal rearrangements, including those that are (moderately) underdominant, may fix or have fixed. A single dagger represents the situation where only chromosomal rearrangements with lower direct fitness costs may fix or have fixed. These pathways are illustrative and are a simplification of the real world: other paths are possible in which the various processes occur in different combinations or sequences. Abbreviations and definitions: DMI: Dobzhansky–Muller incompatibility; LA: local adaptation; MGM: mixed geographic model (Feder et al., 2011); K&B: Kirkpatrick and Barton (2006) model; N&B: Navarro and Barton (2003a) model; Noor: Noor et al.’s (2001) model; Rieseberg: Rieseberg’s (2001) model; White: White’s (1978) stasipatric or similar ‘hybrid-dysfunction’ model.

establishment of different categories of reproductive barrier that different models predict is, however, uncertain. To mention just two examples, one could propose that ecological divergence may contribute to the establishment of CRs (sensu Kirkpatrick and Barton, 2006), which in turn, may lead to the accumulation of genetic incompatibilities (sensu Navarro and Barton, 2003a) that subsequently promote reinforcement. Alternatively, underdominant rearrangements might themselves contribute to post-zygotic isolation, which paves the way for reinforcement to evolve (Stathos and Fishman, 2014). We present some possibilities in Figure 2.

Evidence for the Role of CRs in Speciation Despite interest in the role of CRs in speciation for nearly a century, their role in reproductive isolation is still unclear. One

common finding is an association between karyotypic differences and the opportunity for gene flow between taxa. Such a relationship has been observed at least in Drosophila (Noor et al., 2001), butterflies (Kandul et al., 2007), estrildid finches (Hooper and Price, 2015), and mice (Castiglia, 2014). However, this does not distinguish among models and many challenges remain. The different mechanisms by which CR might contribute to speciation are associated with different geographic scenarios (Figure 2). For instance, most hybrid-dysfunction models assume strong underdominance or multiple weakly underdominant rearrangements that accumulate in the absence of gene flow until their combined effect is negative enough to act as a barrier on secondary contact (Rieseberg, 2001). However, there is now convincing evidence that gene flow during speciation is not as rare as previously thought (Pinho and Hey, 2010) and this is the situation in which

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suppressed-recombination models are more likely to apply. In fact, the growing interest in understanding how speciation occurs in the face of gene flow may have contributed to a bias in the recent literature on CRs and speciation, which tend to be directed toward testing the predictions of suppressedrecombination models. Although many closely related species show fixed CR differences (see above), empirical evidence for their role in reducing gene flow between natural populations and in the establishment of reproductive isolation in nature has been collected for only a handful of cases: in Drosophila (Noor et al., 2001; Kulathinal et al., 2009) sunflowers (Rieseberg et al., 1999; but see Strasburg et al., 2009), apple maggot flies (Feder et al., 2003; Feder et al., 2005), mosquitoes (Ayala and Coluzzi, 2005; Manoukis et al., 2008; Ayala et al., 2013), mice (Panithanarak et al., 2004; Franchini et al., 2010; Giménez et al., 2013), shrews (Basset et al., 2006; Yannic et al., 2009), and plants of the genus Mimulus (Lowry and Willis, 2010; Stathos and Fishman, 2014). In many cases though, we still lack the information needed to form a complete picture of the processes by which CRs have contributed to speciation. Among the model systems that have contributed the most to our understanding of the role of CRs in speciation, the D. pseudoobscura complex is perhaps the best characterized. Drosophila persimilis and D. pseudoobscura are sister species native to North America that started to diverge around 500 000 years ago and now have overlapping ranges (Noor et al., 2001). They differ by three fixed (or nearly) inversions, two on the X chromosome and another on chromosome 2. Despite showing strong reproductive barriers (pre- and post-zygotic), they still hybridize in nature, although rarely (Noor et al., 2001). Remarkably, all the reproductive barriers identified between these two species map exclusively to a few regions on chromosomes X and 2 in or near the inversions. In comparison, isolation loci identified between allopatric species pairs, such as between D. persimilis and D. pseudoobscura bogotana, are mostly located in collinear regions (Brown et al., 2004; Chang and Noor, 2007). This suggests that reproductive barriers mapping to collinear regions between D. persimilis and D. pseudoobscura were eliminated in the face of gene flow, in contrast with those mapping to inversions, which have survived. Consistent with this pattern, divergence between these species is higher within inversions, whereas evidence for introgression is found in collinear regions (Machado et al., 2002; Machado et al., 2007), a trend that is not observed when comparing allopatric populations/species pairs and sympatric pairs where hybridization does not occur, such as between D. persimilis–D. pseudoobscura and Drosophila miranda (Kulathinal et al., 2009; McGaugh and Noor, 2012). Higher divergence within CRs compared with collinear regions was also observed between humans and chimpanzees when this prediction was first tested (Navarro and Barton, 2003b). However, this trend was not confirmed by subsequent studies, some based on full genome data (Zhang et al., 2004; Mikkelsen et al., 2005; Marques-Bonet et al., 2007). Contradictory evidence has also been obtained in terms of higher divergence in gene expression patterns within CRs (Karaman et al., 2003; Zhang et al., 2004; Marquès-Bonet et al., 2004). All this contributes to the overall impression of a minor role of chromosomal speciation in primates and, furthermore, it

illustrates the complications of using solely divergence measures as evidence for the role of CRs in speciation. The difficulties in the study of speciation in the human lineage are indeed considerable. First, since our species and chimpanzees diverged about 4.5–6 million years ago (Locke et al., 2011), the many other evolutionary processes that occurred since their split (including speciation processes) have shaped the divergence landscape (Ayala and Coluzzi, 2005). Second, the impossibility of mapping studies precludes obtaining the sources of evidence that are so helpful in, for instance, Drosophila studies. Finally, inversions could have been segregating before speciation started and thus higher divergence within CRs would not necessarily be associated with speciation (Noor and Bennett, 2009). Thus, despite enormous interest, we are still far from understanding the role that CRs have played in the speciation of humans and chimpanzees, or generally in speciation processes across the primate order. Still, structural variation is known to be high in this taxonomic group (Yunis and Prakash, 1982; Carbone et al., 2014; Rogers and Gibbs, 2014) and is likely to have played a role in primate diversification. Perhaps the best way forward is to focus on recently diverged taxa or those with ongoing gene flow. A more compelling example of the role of CRs in speciation can be found in the yellow monkeyflower, Mimulus guttatus. A perennial ecotype of this species is found in cool, wet coastal conditions, and an annual ecotype is found in inland habitats which experience a summer drought, both in Western North America (Hall and Willis, 2006; Lowry and Willis, 2010). These ecotypes differ in flowering time and morphology, and in other floral, vegetative, and life-history traits (Hall and Willis, 2006). An adaptive shift in flowering time has resulted in temporal pre-zygotic isolation between the two ecotypes. Immigrants are also selected against because of their maladaptive life-history traits (Hall and Willis, 2006). Fascinatingly, Lowry and Willis (2010) found that quantitative trait loci (QTL) for multiple relevant traits map to a chromosomal inversion which is polymorphic within M. guttatus, and which is in perfect association with the contrasting life histories of the perennial and annual ecotypes. Crossing experiments demonstrated that the effects of the inversion are independent of the wider genomic background, and reciprocal transplant experiments showed that the inversion contributes to local adaptation, which in turn causes reproductive isolation as described above (Lowry and Willis, 2010). Elsewhere in the genome variation is most strongly related to geography, which suggests that the inversion is maintaining adaptive polymorphism in the face of strong gene flow (Twyford and Friedman, 2015).

Concluding Remarks Speciation is a process that extends over many generations. During this time, environments and species distributions change, altering population sizes, selection pressures, and opportunities for gene exchange (Abbott et al., 2013). The accumulation of barriers to gene flow is, therefore, likely to occur at an uneven pace, even with existing barriers being lost in some cases, and to be influenced by multiple processes. Where do CRs fit into this picture?

Speciation, Chromosomal Rearrangements and

CRs are simply one class of genetic variant. Any new variant with a negative effect on fitness as a heterozygote will be unlikely to spread and so its potential to contribute to isolation between populations fixed for different variants will only be realized under a restrictive set of conditions. These conditions are far more relaxed for variants with small effects in the genetic background on which they arise but with strong epistatic effects when they meet a different background through hybridization, as in the classic Dobzhansky–Muller model (Gavrilets, 2004). In these respects, CRs are no different unless they are particularly likely to fall into the latter class (as with monobrachial homology of chromosomal fusions, perhaps) or have special features, such as meiotic drive. These features are likely to be common only for some rearrangements and in some taxa (as would also be the case for most classes of genetic variants) suggesting that CRs in general do not play a special role in speciation via these routes. However, CRs are special because of their effects on recombination. These effects vary across classes of rearrangements, with strong reduction in inversion heterokaryotes and new linkage patterns in translocations and fusions. Other classes of genetic variation can also modify recombination (Butlin, 2005; Baudat et al., 2010) but, nevertheless, recombination reduction is a general property of CRs that may impact speciation. Because strong reproductive isolation depends on the build-up and maintenance of associations among traits that contribute barriers to gene flow, suppression of recombination between genes coding for these traits can facilitate speciation (Smadja and Butlin, 2011). The models discussed above show how recombination suppression can make the spread of new CRs more likely (Kirkpatrick and Barton, 2006), how this can result in the more rapid accumulation of both intrinsic and extrinsic reproductive isolation (Rieseberg, 2001; Navarro and Barton, 2003a) and how CRs can protect existing combinations of alleles that contribute to isolation from being disrupted by gene flow (Noor et al., 2001). Current empirical evidence strongly supports an association between CRs and barriers to gene flow. It would be good to extend the comparative evidence from Drosophila (Noor et al., 2001) to more species and other taxa. Case studies show that genic differentiation in the face of gene flow is greater in or near CRs than elsewhere in the genome and that multiple traits associated with barriers to gene flow (intrinsic and extrinsic, pre- and post-zygotic) map to CRs, sometimes exclusively (Noor et al., 2001; Lowry and Willis, 2010). However, it is rare for these studies to go from observing this association to dissecting its origin. We see potential using recently developed approaches to go further in two ways: understanding the relative timing of historical events and identifying loci within CRs that underlie the effect of recombination suppression on reproductive isolation. Comparative analyses and modeling can address critical questions about the origin of CRs in relation to periods of allopatry and secondary contact, or in relation to the origin of adaptive alleles within CRs. Answers to these questions are critical to distinguishing the contributions of the various possible recombination suppression effects. The example of D. pseudoobscura and D. persimilis shows how comparisons among geographic regions and with outgroup species can help in unveiling the sequence of events (Kulathinal et al.,

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2009; McGaugh and Noor, 2012). Recent work on Drosophila mojavensis and Drosophila arizonae using genome sequence data places the origin of inversions at the time of species divergence as well as demonstrating their impact on subsequent introgression (Lohse et al., 2015). Approaches of this type have great potential for application to other systems. Finding the genes that matter within CRs has always been a problem. The suppression of recombination usually precludes classical mapping approaches and compromises genome-scan methods. Low levels of double crossovers and gene conversion may actually hold background differentiation within inversions at low enough levels to detect excess divergence at selected loci (Feder and Nosil, 2009; Stevison et al., 2011; Guerrero et al., 2012). More formal models are needed to understand these processes and make predictions for empirical tests. There is also potential to use gene expression, now readily available through deep-sequencing techniques, to identify candidate loci within inversions. This approach has started to produce interesting insights into candidate loci for adaptation in large-scale inversion clines (e.g., Zhao et al., 2015) but, to our knowledge, it has yet to be applied to the role of CRs in reproductive isolation. If candidates can be identified then, at least in principle, their effects on phenotypes and on reproductive isolation can be tested using RNA interference (Mohr et al., 2014) or genome editing (Harrison et al., 2014) methods while coalescent approaches can be used to test the ages of selective sweeps. In these ways, it may finally be possible to say which loci diverged before and which after the origin of the rearrangements, through which traits they contribute to fitness and to barriers to gene flow and whether their effects on fitness are independent or epistatic. We will then have a full picture of the role of CRs in speciation.

Acknowledgments We thank Graciela Sotelo for her suggestions on a previous version of this manuscript. RF is financed by FCT under the Programa Operacional Potencial Humano – Quadro de Referência Estratégico Nacional from the European Social Fund and the Portuguese Ministério da Educação e Ciência through the postdoctoral fellowship SFRH/BPD/89313/2012. BJ is supported by a PhD studentship, jointly funded by the National Environmental Research Council (NERC) (NE/ H524881/1 and NE/K500914/1) and the Department of Animal and Plant Sciences, University of Sheffield. RKB is funded by NERC and by the Waernska Guest Professorship of the University of Gothenburg.

See also: Reproductive Isolation, Postzygotic. Species Concepts and Speciation

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Further Reading Dobzhansky, T., Sturtevant, A.H., 1938. Inversions in the chromosomes of Drosophila pseudoobscura. Genetics 23 (1), 28–64. Hoffmann, A.A., Rieseberg, L.H., 2008. Revisiting the impact of inversions in evolution: From population genetic markers to drivers of adaptive shifts and speciation? Annual Review of Ecology, Evolution, and Systematics 39, 21–42.

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Kirkpatrick, M., Barton, N., 2006. Chromosome inversions, local adaptation and speciation. Genetics 173 (1), 419–434. Lohse, K., Clarke, M., Ritchie, M.G., Etges, W.J., 2015. Genome-wide tests for introgression between cactophilic Drosophila implicate a role of inversions during speciation. Evolution 69 (5), 1178–1190. Lowry, D.B., Willis, J.H., 2010. A widespread chromosomal inversion polymorphism contributes to a major life-history transition, local adaptation, and reproductive isolation. PLOS Biology 8 (9), e1000500. Navarro, A., Barton, N.H., 2003. Accumulating postzygotic isolation genes in parapatry: A new twist on chromosomal speciation. Evolution 57 (3), 447–459.

Noor, M.A.F., Grams, K.L., Bertucci, L.A., Reiland, J., 2001. Chromosomal inversions and the reproductive isolation of species. Proceedings of the National Academy of Sciences of the United States of America 98 (21), 12084–12088. Rieseberg, L.H., 2001. Chromosomal rearrangements and speciation. Trends in Ecology and Evolution 16 (7), 351–358. Stevison, L.S., Hoehn, K.B., Noor, M.A.F., 2011. Effects of inversions on within- and between-species recombination and divergence. Genome Biology and Evolution 3, 830–841. Trickett, A.J., Butlin, R.K., 1994. Recombination suppressors and the evolution of new species. Heredity 73 (4), 339–345.