Genetic Introgression: An Integral but neglected component of speciation in birds

Abstract

HYBRIDIZATION, OR THE act of reproduction between different species, is common in birds (Grant and Grant 1992) and can be an agent of adaptive evolution (Veen et al. 2001). When hybridization occurs, a species' genetic material may enter the gene pool of another and thereby introduce genetic novelty. This process is called “genetic introgression” (hereafter “introgression”; Anderson 1949). Although known for decades, the incidence of introgression in nature has long been underappreciated (e.g., Currat et al. 2008). Only recently have evolutionists come to regard it as an important and pervasive mechanism in speciation, in the maintenance of genetic diversity and in the introduction of advantageous novelty into the gene pool (Arnold et al. 1999, Noor et al. 2000, Seehausen 2004). In fact, genetic data now suggest that our own species may have undergone a complicated history of introgression with at least two extinct hominine lineages (Green et al. 2010, Reich et al. 2010). Another reason why introgression is an important topic is the impact of human-induced climate change, which is rapidly shifting vegetation boundaries and creating new hybrid zones, with little-known consequences for the genetic integrity of species (Mank et al. 2004, Brumfield 2010). There has been a tremendous increase in introgressionrelated avian research since a comprehensive overview of the introgression complex between the Blue-winged Warbler (Vermivora cyanoptera) and the Golden-winged Warbler (V. chrysoptera) appeared in The Auk five years ago (Confer 2006). Here, we seek to fill a gap by summarizing the most important recent advances in avian introgression research and our current understanding of locus-specific differences in introgression dynamics, the detection of introgression, its directionality, and its relevance to conservation, phylogenetics, and speciation research. Different DNA classes are expected to vary in their potential to introgress between species. One reason is “Haldane's rule,” which predicts that heterogametic hybrid offspring are often less viable or fertile (Haldane 1922). The basis of Haldane's rule seems to lie in the recessiveness of alleles that decrease hybrid fitness, such that, say, the ZW sex suffers more than the ZZ sex because Z-linked alleles causing postzygotic isolation tend to have greater cumulative effects when hemizygous than when heterozygous (“dominance theory”; Turelli and Orr 1995). In birds, females are the heterogametic sex (ZW), and experiments in ducks have empirically confirmed female hybrid inviability (Kirby et al. 2004). In the absence of positive selection, we can thus predict that mitochondrial DNA (mtDNA) and W-linked DNA, which are female-transmitted, are not as likely to introgress as Z-Iinked DNA and are even less likely to introgress than autosomal DNA. In one of the earliest avian introgression studies, Tegelström and Gelter (1990) interpreted differences in interspecific divergence between mtDNA and nuclear DNA (nDNA) in a European flycatcher (Flcedula) hybrid zone as a sign of nuclear introgression. Even in the absence of introgression, divergence patterns between mtDNA and nDNA often differ because of the evolutionary properties of these DNA classes. However, the Ficedula hybrid zone has by now become a model system for the investigation of differential introgression among DNA classes, and Tegelström and Gelter's (1990) initial suspicions of species-wide nDNA introgression have been confirmed (Sætre et al. 2001, 2003). Comparisons of the incidence of introgression between sexlinked and autosomal markers seem to demonstrate that the Z chromosome in Ficedula and other birds is particularly impermeable to introgression, perhaps more so than predicted by Haldane's rule (Sætre et al. 2003, Borge et al. 2005b, Carling and Brumfield 2008, Carling et al. 2010, Storchová et al. 2010). Flycatchers in the genus Ficedula exhibit plumage character displacement where species overlap, albeit at different regional intensities (Borge et al. 2005a). At the same time, their plumage characters and femalechoice characters are Z-linked and under selection (Sætre et al. 2003, Sæther et al. 2007, Backström et al. 2010a). This simultaneous Z linkage, coupled with potentially reduced rates of recombination on the female Z chromosome, is a strong argument in favor of prezygotic factors playing a role in reduced Z introgression. This is all the more plausible considering that Backström et al. (2010b) tested and rejected a competing hypothesis that rearrangements in the Ficedula Z chromosome account for its impermeability to introgression. On the other hand, many other avian hybrid zones do not exhibit character displacement and may lack these special conditions of Ficedula gene arrangement. This suggests that postzygotic factors may be equally important in reducing levels of Z introgression. Indeed, Ellegren (2009) proposed an accelerated rate of adaptive divergence of Z-linked loci compared with autosomal loci (“large-Z effect”), suggesting that the Z chromosome is particularly impermeable to introgression because it holds a disproportionately high number of loci that may be subject to the dynamics of dominance theory (Turelli and Orr 1995). The large-Z effect is supported by recent work on a Z-linked locus involved in egg-laying characters: Carling and Brumfield's (2009) study of a hybrid zone between two bunting species (Passerina) showed that the foreign allele (i.e., typical for the rarer species at any given locality in the hybrid zone) is selected against, prompting the authors to suggest that the Z chromosome may be a hotspot for “speciation genes” that are linked to reproductive isolation. Many studies that have sampled both mtDNA and nDNA across avian hybrid zones have retrieved the pattern of increased nDNA versus mtDNA introgression predicted by Haldane's rule. Mammals exhibit the opposite pattern, presumably because of their male heterogamety (Petit and Excoffier 2009). Disregarding cases of geographically widespread introgressive mtDNA sweeps for the moment, levels of mtDNA introgression in avian hybrid zones are often low or zero (Tegelström and Gelter 1990; Helbig et al. 2001, 2005; Sætre et al. 2001, 2003; Bensch et al. 2002; Crochet et al. 2003; Kvist and Rytkönen 2006; Secondi et al. 2006; Martínez-Cruz and Godoy 2007; Vallender et al. 2007; Carling and Brumfield 2008; Rush et al. 2009) or are at least accompanied by equivalent levels of nDNA introgression (Brumfield et al. 2001, Gay et al. 2008, Rheindt et al. 2009). Studies on ducks in the genus Anas may show an opposite trend (McCracken et al. 2001; Kulikova et al. 2004, 2005; Peters et al. 2007)—similar to that in that introgression to be more in mtDNA than in and Excoffier (2009) for by in which with in most other the incidence of mtDNA versus nDNA introgression in ducks is different that in other birds, and and (2009) for is to be tested with data that both mtDNA and nDNA theory predicts reduced levels of introgression in avian mtDNA and loci as compared with autosomal loci on the basis of the of heterogametic (Turelli and Orr 1995). However, holds for loci that are not under The of is often particularly for in the patterns expected for a Haldane's positive selection can mtDNA introgression hybrid zones and to sweeps across species for loci under and positive of species and with a hybrid zone in positive selection, the of species the of species and the introgression be to the hybrid zone in in that genetic can account for genetic sweeps in into differences in introgression potential among and mtDNA loci is an of in both model and species. At the same time, studies on birds have an important role in in the of introgression not among among autosomal loci (e.g., Borge et al. Kvist and Rytkönen Secondi et al. Martínez-Cruz and Godoy 2007, Peters et al. 2007, Vallender et al. 2007, Carling and Brumfield 2008, Gay et al. 2008, Carling et al. 2010). among autosomal loci sampled across a hybrid Carling et al. differences of more than an of in levels of and these to locus-specific differences in introgression. However, many studies have been to a or nuclear a of that it to the of differences in introgression potential among autosomal In the of autosomal loci in hybrid zone studies may be by the of markers that show strong which can in an in the of patterns (Brumfield et al. 2001, et al. 2009). when be to with patterns of such as we may the of differential introgression among autosomal et al. that differential introgression may be a process by considering and potentially differences in introgression patterns between different DNA classes it is plausible to that may account for locus-specific differences such genetic may the or of introgression the selected locus to as has been proposed by et al. for a hybrid This introgression hypothesis has for birds in the of may be to with the of in avian evolutionary research. a hybrid zone that seems to to introgression of loci that recombination may be these et al. The most to study introgression is across a hybrid zone where two species come into and in levels of even in a hybrid zone it is to patterns of DNA as introgression. of may be to with DNA et al. zones are often in which selection the of alleles across species (e.g., Kvist and Rytkönen 2006; Carling and Brumfield 2008; Gay et al. 2008, et al. and 2009). or reproductive a hybrid zone can be to a by the genetic integrity of the species on is to female hybrid inviability Haldane's rule. However, is that a of other factors may at a and selection in and that to may be an important in a hybrid In it may be or selection that for reduced reproductive in et al. prezygotic and postzygotic factors may be important in a hybrid on the model species. often at the of where have a of their own species. special of process on in the which recently by an and a species of to a that genetic to both species et al. 2010). are with a in which one species the other in (e.g., et al. 2001, et al. 2004, Secondi et al. Gay et al. 2008). In most of these of the species the of the hybrid zone and an of hybrid In hybrid zones, introgression may at such a that can be the of The between a subject to introgression versus one that has become a new hybrid species seems to on reproductive isolation both species is et al. Although of speciation has long been in birds, et al. recently that the an number of with both of its species, the and This seems to the on the as a avian hybrid species. of potential hybrid speciation the Warbler which the Warbler its mtDNA and a hybrid zone with the Warbler and et al. et al. In of nuclear Warbler a of Warbler the hybrid research on the zone between and to is reproductive isolation between to Warbler as a hybrid species, as to a that is with the albeit with Warbler DNA. On a hybrid zones often geographically among different of among hybrid zones are called The where and species come into is one of the most important (e.g., Carling and Brumfield 2008, and Carling and Carling et al. Many hybrid zones are known to an hypothesis is of a zone in the same thereby to a of the zone (e.g., as seems to be the in the Carling and The have important for our into the role of factors as climate in species has long been as in species boundaries in it has been less of an in (e.g., Even avian have low to and of these are now known to be subject to complicated patterns of introgression. such a complex in which species may with other on important model system has hybrid speciation (Grant and Grant the of on introgression (Grant et al. speciation et al. and the of introgression in the introduction of genetic novelty (Grant and Grant 2010). is so in that species boundaries have been The and is another that in complicated patterns of introgression (McCracken et al. 2001; Kulikova et al. 2004, species of in the genus exhibit an pattern of introgression et al. 2004, et al. et al. 2009). Although the of introgression and the of in have been the seems so complex that nDNA data across many of the and demonstrate that avian introgression may hybrid that often in complicated avian are not the complicated introgression less are known in which hybridization with low mtDNA predict work et al. and birds such as et al. 2010). Studies of avian hybrid zones suggest that introgression can be one species to the other not (e.g., Sætre et al. 2003, Grant et al. 2004, Borge et al. Helbig et al. Storchová et al. 2010). In shifting hybrid zones, introgression has been to the to the that introgression into the of the species (e.g., et al. 2001, Secondi et al. et al. 2010). One potential to the pattern expected for introgression et al. in which hybrid have the nuclear of the species the mtDNA of the On the basis of of with et al. interpreted pattern as mtDNA introgression the a pattern that with the in most other avian However, because seem to in the hybrid pattern equally be interpreted as nuclear introgression into a that is to the hybrid into a with of the a pattern in other birds and and known as a of introgression do of introgression come into introgression is at the species, we be to the DNA of species to that as hybrid zones In birds, pattern in a study of the and hybrid zone by et al. showed that the Warbler a of its in the of that now its There is reason to that Warbler mtDNA is it by now have Warbler mtDNA its not across the of This of process may be widespread and is one of a in which introgression can hybrid zones positive selection study of in the genus suggests that the most in that have (i.e., the of the Secondi et al. 2006). for a locus in a hybrid The the hybrid zone between species and The the of hybrid zone The versus the typical for species and the of species species a genetic of its introgression. The can be to patterns of character across other avian hybrid zones such as that of Brumfield et al. in which mtDNA and nDNA markers of into the of birds that exhibit the plumage of Carling and Brumfield (2009) that Z-Iinked introgression into may be a of the in the of a hybrid that the is that species may the of another species that has long since (e.g., as a of a hybrid zone that has its and one of the species to be to because the species is to cases may to species that two and mtDNA such as the et al. which may have one of its mtDNA another it has long since studies to introgression into species, are these in with by Currat et al. introgression of loci into species across shifting hybrid that the most important for introgression in a hybrid zone is the of the species, where is an initial between a low number of and a number of In initial hybridization may be to the species in the of the species and the of the is by a effect Although selection on at least a of loci be involved in the of one species at the of the Currat et that selection not be as the conditions at the of markers to to high of Currat et for a locus with a different allele typical for species. is a of is species is and are in of the allele of species at the locus allele and the allele to species allele species is with species of species into the of species The may have allele a or allele in hybrid allele is likely to because of allele a are in the at the of of species are at the as the of the the initial between and common allele to to at the time, the of species is at the it alleles as the one in in the new of introgression. is that introgression may to a of genetic integrity of species are by study by for on a of in the mtDNA may be rapidly by that of the Blue-winged However, studies in system have been more mtDNA introgression seems to be more or less most et al. 2004, et al. foreign nDNA may into the et al. not into the Although Vallender et hybrid zone Golden-winged on of the one Blue-winged Warbler of which suggests introgression rates into the introgression often in a hybrid zone to the of a of genetic of the gene pool may often be so long as of where the shifting hybrid zone has not The to species hybrid zones have to the of the species' and are to the et al. the when a widespread species, the may have been to its The that has the recent of of mtDNA and perhaps not the of the model et al. 2008). the is now reduced to a and a of to a of and a of the et al. 2010). The species process of hybrid zones is a common evolutionary it is plausible to that on the may the of hybrid zones or new On an evolutionary our of be low not in the study of introgression in Anas the of a of the and the their to (Mank et al. 2004). In another et al. a of years to demonstrate that the hybrid zone between two European is and is rapidly At the of the process is expected on a of to of different is by the of with In introgression is not to the as in the is by of hybridization the of a species, such as the of et al. such a in where nDNA introgression into showed for the genetic integrity of the nuclear markers are known for their incidence of introgression across avian hybrid zones compared with mtDNA with Haldane's In mtDNA is known for among the most markers to introgressive and mtDNA sweeps are to a of species that are not known to in hybridization or of species that are any hybrid The of mtDNA introgression in the in et al. and and birds of avian mtDNA introgression and and it has been in most can avian mtDNA be to introgression across hybrid zones because of Haldane's rule on the one hand, to introgressive sweeps on the may be the When a a foreign it to introgress a hybrid zone because genetic its is a between two a foreign allele may rapidly its potentially the one its that the of dynamics has the the The of mtDNA sweeps in the when a female hybrid is to introduce the and advantageous into the species. In many Haldane's female hybrid inviability may not be and the may to On the other hand, of mtDNA may introgressive sweeps in the is to be is to of that the one in birds in a hybrid a zone of introgression et al. 2003). locus under positive selection is of the and its so why is particularly to a (e.g., and mtDNA dynamics are now known to be more complex than on and 2004, et al. 2006). of its role in mtDNA is the subject of sweeps that with properties (e.g., et al. in that across a of and other to in the genus et al. et al. 2003, et al. 2004, et al. and Brumfield 2009). mtDNA sweeps the low of mtDNA diversity that is often species et al. 2006). may be less of an in mtDNA as compared with nuclear markers not because of its because selection can the effects of 2009). The adaptive of mtDNA in the of new in predict that mtDNA sweeps be more common at This may be an in the why birds are more or birds exhibit mtDNA (e.g., and 2004). This hypothesis be nuclear data become more it is that the lack of mtDNA in many and birds, such as et al. and and may have a than a a hypothesis that can be tested with nuclear The of introgressive sweeps is in its because introgression can be and 2003). introgressive sweeps have been when a locus a and different of other loci or characters (e.g., et al. 2001, and 2003, et al. 2007, et al. 2008, et al. 2008, et al. Rheindt et al. 2009). In most of these is to the between mtDNA and often for of that, in introgression is and be a tested hypothesis in the have been proposed by which the hypothesis of introgression can be tested that of In birds, Peters et al. an that a and it to a of mtDNA in two species the of divergence introgression or as an for mtDNA compared these with nDNA This confirmed initial suspicions that mtDNA introgression is the likely of In more complicated as et al. may because it on the that the nDNA markers as a are to introgression. This is by the it to in the less complex Another for introgression is one in which or divergence are not among different loci among different and This that are to be by introgression with that are to be (e.g., Grant et al. a of to show that introgression has of a species compared interspecific between with between that introgression has been pervasive in more complex to of have been for data in introgression among recent lineages of (Green et al. 2010, Reich et al. 2010). The of these in introgression in their on loci that exhibit the in the (i.e., so that any by the two and is likely to be the of data in be tested in for one mitochondrial locus and two nuclear loci and in and is to the number of Peters et al. are to the where In the of in a as as in a by is interpreted as introgression. that the nDNA locus in is to the hypothesis of mtDNA the of introgression. is often when two species exhibit in mtDNA (e.g., et al. 2001, et al. Rheindt et al. is the a of potential introgression. hybridization in the has long since we two species as lineages with effects may have important for divergence when a is on the mtDNA rate of (e.g., and have to many important in However, more and more a may show of these to be the of introgression. both and interspecific sweeps account for a of mtDNA interspecific divergence to so when an mtDNA pattern is introgression be as a is when two or more species are on the basis of when or both may (e.g., et al. 2007, et al. et al. 2010). these studies be is not the since the since the introgressive mtDNA the divergence to can not increase in Many mtDNA studies, the et al. 2007, and 2008, et al. their data for or divergence Although the may be and are often supported by data et al. the may of introgression. et al. 2007, a of species by and a high of species that are known to and in which introgression has been such as ducks (McCracken et al. 2001; Kulikova et al. 2004, 2005; et al. Peters et al. et al. 2004, et al. et al. and et al. 2010). of introgression is that it not a between two species, the introgressive gene a that to be Brumfield et al. in a of the of it to the given that introgression is known to in between and patterns and in the genus et al. 2010, and On the basis of nuclear markers and the is now to be to as and not to the mtDNA it This has for work on the of a between and et al. 2008). introgression and the gene The species is and among lineages and are (i.e., are to introgressive sweeps into species for for introgressive locus are in a introgressive in and both species have since into species, the introgressive may a at The most which an advantageous mtDNA the introgression and 2006). are not of any in which potentially widespread has been in been as one of to the mtDNA to species et al. research by and has its likely for hybridization may be the by mtDNA in that are to with and data et al. 2008, et al. 2008, et al. of the of may be an of introgressive mtDNA in the of patterns be any a is data are because the loci or patterns in loci and an can pervasive mtDNA sweeps it is to cases that their and introgression as one of of gene the other two and to a in which the of a is at with its species The in which of the is causing a arrangement. and (2009) most cases of to introgression or the of and in a of cases of to to to introgression, and to that the low incidence of introgression in avian mtDNA the of mtDNA as a However, and (2009) of the of may have been in two often on the even authors often introgression, and their of on pattern is by introgression in the suggest that introgression may be a more widespread of avian gene than is However, are to the to which introgression speciation the of a into which (e.g., This is in most avian research in that genetic the initial (i.e., is to be introgression may be a of initial and 2003, Seehausen a hypothesis that can be tested with has been a recent of avian studies that for introgression to be into account the initial of species et al. Carling et al. 2010, et al. 2010). the of another in avian evolutionary research is the of into speciation and et al. et al. be a in these it is often by and shifting The years have been by a of and by of and 2001, et al. 2003, et al. and of these or a of by or by a of and by or levels in of and introgression. The of to these into of genetic be a high on the of evolutionary a long time, introgression has been as an in the of to the of the evolutionary of recent that introgression may be an of the evolutionary on genetic on an of has that introgression may have been an important in the evolution of (Green et al. 2010, Reich et al. 2010). introgression is to be an important of the speciation process for other model species for which data have been such as and 2003, et al. 2009) or et al. 2009). such as in the of evolutionary of species (e.g., and 2010, et al. in the study of avian introgression. speciation in the of introgression. of the The speciation model as in most recent research. potentially more in which the two species become and one another with to and introgressive hybridization in The of a of introgression as the two species that model a more recent of speciation than model that model is for species become it can equally be to to species become (e.g., because of with such as in the This research supported by a and by and two for their and which the