Hybrid zone: Difference between revisions
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{{Short description|Population genetics term}} |
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| ⚫ | A '''hybrid zone''' exists where the ranges of two [[interbreeding]] [[species]] or diverged intraspecific lineages meet and cross-fertilize. Hybrid zones can form ''in situ'' due to the evolution of a new lineage<ref name="endler1977">{{cite book|author= Endler, J. |title =Geographic Variation, Speciation and Clines|publisher |
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[[File:Hybrid figure resulting from secondary contact.png|border|right|frameless|315x315px|Hybrid zones can form from secondary contact]] |
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| ⚫ | A '''hybrid zone''' exists where the ranges of two [[interbreeding]] [[species]] or diverged intraspecific lineages meet and cross-fertilize. Hybrid zones can form ''in situ'' due to the evolution of a new lineage<ref name="endler1977">{{cite book|author= Endler, J. |title =Geographic Variation, Speciation and Clines|publisher=Princeton University Press |location=Princeton, NJ|series=Monographs in Population Biology |year =1977|volume=10|pages =1–246|pmid =409931|isbn =9780691081922 |url =https://books.google.com/books?id=BL12fYUMobwC}}</ref>{{Page needed|date=March 2024|reason=Citation listed *all* pages previously. Need page or range for information being cited.}} but generally they result from [[secondary contact]] of the parental forms after a period of geographic isolation, which allowed their differentiation. Hybrid zones are useful in studying the genetics of [[speciation]] as they can provide natural examples of differentiation and gene flow between populations that are at some point on the continuum between diverging populations and separate species with [[reproductive isolation]]. |
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==Definition== |
==Definition== |
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Hybrid zones are |
Hybrid zones are areas where the hybrid offspring of two divergent taxa (species, subspecies or genetic "forms") are prevalent and there is a [[cline (population genetics)|cline]] in the genetic composition of populations from one taxon to the other.<ref name="Barton_Hewitt">{{cite journal |author=[[Nick Barton|N. H. Barton]] & G. M. Hewitt |year=1985 |title=Analysis of hybrid zones |journal=[[Annual Review of Ecology and Systematics]] |volume=16 |pages=113–148 |doi=10.1146/annurev.es.16.110185.000553}}</ref> The two (or more) genetically differentiated species or lineages contributing to formation of a hybrid zone are regarded as parental forms. Precise definitions of hybrid zones vary; some insist on increased variability of [[Fitness (biology)|fitness]] within the zone, others that hybrids be identifiably different from parental forms and others that they represent secondary contact alone.<ref>Murray, 1985{{citation needed|date=June 2012}}</ref> The widths of such zones can vary from tens of metres to hundreds of kilometres.<ref>{{Cite journal |last1=Morgan-Richards |first1=Mary |last2=Wallis |first2=Graham P. |date=2003 |title=A comparison of five hybrid zones of the weta Hemideina thoracica (Orthoptera: Anostostomatidae): degree of cytogenetic differentiation fails to predict zone width. |url=https://academic.oup.com/evolut/article/57/4/849/6756069 |journal=Evolution |language=en |volume=57 |issue=4 |pages=849–861 |doi=10.1111/j.0014-3820.2003.tb00296.x |pmid=12778554 |issn=0014-3820}}</ref> The shape of the zones (clines) can be gradual or stepped.<ref name="Barton_Hewitt"/> Additionally, hybrid zones may be ephemeral or long-lasting.<ref name=":1" /> |
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Some hybrid zones can be seen as presenting a [[paradox]] for the [[biological species concept|biological definition of a species]], usually given as "a population of actually or potentially [[interbreeding]] individuals that produce fertile offspring" |
Some hybrid zones can be seen as presenting a [[paradox]] for the [[biological species concept|biological definition of a species]], usually given as "a population of actually or potentially [[interbreeding]] individuals that produce fertile offspring" <ref>{{cite book |author=Ernst Mayr |year=1942 |title=Systematics and the Origin of Species |url=https://archive.org/details/systematicsorigi0000mayr_p8z7 |url-access=registration |location=New York |publisher=[[Columbia University Press]]|author-link=Ernst Mayr }}</ref> under what has become known as the Biological Species Concept. Under this definition, both parental forms could be argued to be the same species if they produce fertile offspring at least some of the time. However, the two parental populations or species often remain identifiably distinct, conforming to an alternative, and presently preferred concept of species as "taxa that retain their identity despite gene flow".<ref>{{Cite journal |last=Mallet |first=James |date=1995-07-01 |title=A species definition for the modern synthesis |url=https://dx.doi.org/10.1016/0169-5347%2895%2990031-4 |journal=Trends in Ecology & Evolution |volume=10 |issue=7 |pages=294–299 |doi=10.1016/0169-5347(95)90031-4 |pmid=21237047 |issn=0169-5347}}</ref><ref name="Barton_Hewitt"/> |
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The clines of hybrid zones can be observed by recording the frequency of certain diagnostic [[alleles]] or phenotypic characteristics for either population along a transect between the two populations. Often the clines take the form of a |
The clines of hybrid zones can be observed by recording the frequency of certain diagnostic [[alleles]] or phenotypic characteristics for either population along a transect between the two parental populations or species. Often the clines take the form of a sigmoidal curve. They can be wide (gradual) or narrow (steep) depending on the ratio of hybrid survival to recombination of genes.<ref>{{cite journal |author=N. H. Barton |year=1983 |title=Multilocus clines |journal=[[Evolution (journal)|Evolution]] |volume=37 |issue=3 |pages=454–471 |jstor=2408260 |doi=10.2307/2408260|pmid=28563316 |author-link=Nick Barton }}</ref> Hybrid zones which show no regular transition from one taxon to the other, but rather a patchy distribution of parental forms and subpopulations with hybrid background, are termed ''mosaic hybrid zones''.<ref name=":1" /> |
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== Models and theories == |
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===Forms=== |
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Various models and theories have been developed by the researchers of hybrid zones. Major models can be largely categorized into four types: ephemeral hybrid zone theory,<ref name=":0">{{cite journal |author=William S. Moore |year=1977 |title=An evaluation of narrow hybrid zones in vertebrates |url=http://digitalcommons.wayne.edu/cgi/viewcontent.cgi?article=1010&context=biosci_frp |journal=[[Quarterly Review of Biology]] |volume=52 |issue=3 |pages=263–278 |doi=10.1086/409995 |jstor=2824163 |s2cid=14462807}}</ref> bounded hybrid superiority model,<ref name=":0" /> mosaic hybrid zone model<ref name=":1">{{Cite journal |last=Harrison |first=Richard |date=1990 |title=Hybrid zones: windows on evolutionary process |journal=Oxford Surveys in Evolutionary Biology |volume=7}}</ref> and tension zone model.<ref name="Barton_Hewitt" /> In each model, different evolutionary forces are attributed different levels of importance. The different models result largely from the study of different biological material (natural populations). The four major models operate mostly under a general framework of either a balance between natural selection and dispersal or interaction between genotypes and environment.<ref name=":3">{{Cite book |last=Arnold |first=Michael L. |title=Natural hybridization and evolution |date=1997 |publisher=Oxford University Press |isbn=978-0-19-509974-4 |series=Oxford series in ecology and evolution |location=New York Oxford}}</ref> Different hybrid zones may fit different models and no single theory or model serves to explain all the hybrid zones found in nature. |
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| ⚫ | Hybrid zones can be either ''primary'' or ''secondary''. |
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| ⚫ | One form of hybrid zone results where one species has undergone [[allopatric speciation]] and the two new populations regain contact after a period of geographic isolation. The two populations then mate within an area of contact, producing 'hybrids' which contain a mixture of the alleles distinctive for each population. Thus novel genes flow from either side into the hybrid zone. Genes can also flow back into the distinct populations through interbreeding between hybrids and parental (non-hybrid) individuals ([[introgression]]).<ref>{{cite book |author= |
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Some early evolutionary biologists who preferred a biological species concept, such as [[Ernst Mayr]]<ref>{{Cite book |last=Mayr |first=Ernst |url=https://books.google.com/books?id=mAIjnLp6r_MC |title=Systematics and the Origin of Species, from the Viewpoint of a Zoologist |date=1999 |publisher=Harvard University Press |isbn=978-0-674-86250-0 |language=en}}</ref> and [[Theodosius Dobzhansky]],<ref>{{Cite journal |date=July 1940 |title=Speciation as a Stage in Evolutionary Divergence |url=https://www.journals.uchicago.edu/doi/10.1086/280899 |journal=The American Naturalist |language=en |volume=74 |issue=753 |pages=312–321 |doi=10.1086/280899 |issn=0003-0147}}</ref> believed that hybrid zones are generally rare and ephemeral, with an eventual fate of either merging of the hybridizing populations or reinforcement, which leads to a speciation event. The extinction of one of the hybridizing populations through introgression is sometimes termed “waves of advance”.<ref name=":4">{{Citation |last=Harrison |first=Richard G |title=Hybrids and Hybrid Zones: Historical Perspective |date=1993-06-17 |work=Hybrid Zones and the Evolutionary Process |pages=3–12 |url=https://doi.org/10.1093/oso/9780195069174.003.0001 |access-date=2024-03-22 |publisher=Oxford University PressNew York, NY |doi=10.1093/oso/9780195069174.003.0001 |isbn=978-0-19-506917-4}}</ref> (Although this term can also refer to the spreading of advantageous allele across a reproductive barrier<ref>{{Cite journal |last=FISHER |first=R. A. |date=June 1937 |title=The Wave of Advance of Advantageous Genes |journal=[[Annals of Eugenics]] |volume=7 |issue=4 |pages=355–369 |doi=10.1111/j.1469-1809.1937.tb02153.x |issn=2050-1420|doi-access=free|hdl=2440/15125 |hdl-access=free }}</ref>) The ephemerality of hybrid zone has been countered by the discovery of many hybrid zones that has lasted for a long period of time,<ref name=":0" /> up to 100,000 years found between the iguanid lizards, ''Sceloporus woodi'' and ''S. undulatus undulatus''.<ref>{{Cite journal |last=Jackson |first=James F. |date=1973-03-01 |title=The Phenetics and Ecology of a Narrow Hybrid Zone |url=http://dx.doi.org/10.1111/j.1558-5646.1973.tb05917.x |journal=Evolution |volume=27 |issue=1 |pages=58–68 |doi=10.1111/j.1558-5646.1973.tb05917.x |pmid=28563661 |issn=0014-3820}}</ref> |
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=== Bounded hybrid superiority === |
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Hybrid zones and gene flow do not inevitably lead to merging of the two populations involved, and some hybrid zones may be retained for thousands of years.<ref>{{cite journal |author=M. J. D. White, R. E. Blackith, R. M. Blackith & J. Cheney |year=1967 |title=Cytogenetics of the ''viatica'' group of morabine grasshoppers. I. The "coastal" species |journal=[[Australian Journal of Zoology]] |volume=15 |issue=2 |pages=263–302 |doi=10.1071/ZO9670263}}</ref> Some persistent hybrid zones are 'tension zones', where the conflicting effects of dispersal of parental forms and selection against hybrids balance each other.<ref>{{cite journal |author=A. D. Bazykin |year=1969 |title=Hypothetical mechanism of speciation |journal=[[Evolution (journal)|Evolution]] |volume=23 |issue=4 |pages=685–687 |jstor=2406862 |doi=10.2307/2406862}}</ref> Dispersal of individual parents leads to the creation of more hybrids within the hybrid zone. This may result in gene flow between the two populations because of introgression. However, in the tension zone model hybrids are less fit than parental forms (perhaps because they lack the complete [[gene complexes]] of the parentals that make them well adapted to the environments either side of the hybrid zone), or even inviable or sterile. Inviability or [[infertility|sterility]] of hybrids forms a barrier to gene flow by making a 'hybrid sink' into which genes from parentals flow but rarely continue into the other population. Statistical models suggest that neutral alleles flow across this barrier very slowly while positively selected alleles will move across quite rapidly.<ref name="Barton_Hewitt"/> An interesting outcome of this model is that tension zones are almost environment independent and can therefore move<ref>{{cite journal |author=[[Nick Barton|N. H. Barton]] |year=1979 |title=The dynamics of hybrid zones |journal=[[Heredity (journal)|Heredity]] |volume=43 |pages=341–359 |doi=10.1038/hdy.1979.87}}</ref> and empirical cases of this have been found.<ref>{{cite journal |author=[[Richard Buggs]] |year=2007 |title=Empirical study of hybrid zone movement |journal=[[Heredity (journal)|Heredity]] |volume=99 |pages=301–312 |doi=10.1038/sj.hdy.6800997}}</ref> |
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The ''bounded hybrid superiority model'' predicts that hybrids have higher fitness in a habitat that is intermediate between those of their parental populations.<ref name=":0" /> The hybrid habitat occurs usually, but not necessarily, on a narrow [[ecotone]]. Clines of a bounded hybrid superiority zone reflect a smooth gradient corresponding to the gradient of differential selection strength in fitness-related characteristics.<ref name="Barton_Hewitt" /> The bounded superiority model places a high importance on the ecological aspect of the habitat. In fact, botanist [[Edgar Anderson]] suggested that hybrid populations are more likely to inhabit ecologically disturbed areas, which often occur under human’s modification of landscapes or geological events that create novel habitat conditions.<ref name="Barton_Hewitt" /> He argued that hybrid zones are essentially formed via “hybridization of habitats”.<ref>{{Cite journal |last=Anderson |first=Edgar |date=1948 |title=Hybridization of the Habitat |url=https://www.jstor.org/stable/2405610 |journal=Evolution |volume=2 |issue=1 |pages=1–9 |doi=10.2307/2405610 |jstor=2405610 |issn=0014-3820}}</ref> Anderson also considered natural hybridization as a positive evolutionary stimulus that allows different populations and lineages to exchange adaptive genetic elements<ref>{{Cite journal |last1=Anderson |first1=E. |last2=Stebbins |first2=G. L. |date=1954 |title=Hybridization as an Evolutionary Stimulus |url=https://www.jstor.org/stable/2405784 |journal=Evolution |volume=8 |issue=4 |pages=378–388 |doi=10.2307/2405784 |jstor=2405784 |issn=0014-3820}}</ref>—similar view that place a high evolutionary importance on hybrid zones is more prevalent among botanists, in contrast to zoologists who are more likely see hybrid zones as more of a “natural laboratory” of population genetics.<ref name=":4" /> Some criticism for the bounded superiority model suggests that hybrid zones with higher hybrid fitness are theoretically unlikely to be distributed along narrow ecotones;<ref name=":2">{{Cite journal |last1=Barton |first1=N. H. |last2=Hewitt |first2=G. M. |date=1985 |title=Analysis of Hybrid Zones |url=https://www.jstor.org/stable/2097045 |journal=Annual Review of Ecology and Systematics |volume=16 |pages=113–148 |doi=10.1146/annurev.es.16.110185.000553 |jstor=2097045 |issn=0066-4162}}</ref> some also point out that there has not been direct empirical evidence of higher hybrid fitness along an ecological gradient (i.e. ecotones).<ref name=":1" /> |
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=== Tension zone model === |
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Another model for a persistent hybrid zone is the ecotonal model, in which a hybrid zone occurs over an environmental gradient with each parental lineage being adapted to one part of that gradient. The frequency of alleles finding different equilibria therefore depends on the precise environmental conditions in a particular area. In each location, selection maintains a stable equilibria for each allele, resulting in a smooth cline.<ref>{{cite journal |author=William S. Moore |year=1977 |title=An evaluation of narrow hybrid zones in vertebrates |journal=[[Quarterly Review of Biology]] |volume=52 |issue=3 |pages=263–278 |jstor=2824163 |doi=10.1086/409995}}</ref> The hybrids must therefore be fitter at some point along the cline. Another model is the wave of advance model that sees multiple clines for individual alleles forming due to the progression of advantageous alleles from one population the other.<ref>{{cite journal |author=Jaroslav Pialek & [[Nick Barton|Nick H. Barton]] |year=1997 |title=The spread of an advantageous allele across a barrier: the effects of random drift and selection against heterozygotes |journal=[[Genetics (journal)|Genetics]] |volume=145 |issue=2 |pages=493–504 |pmid=9071602 |pmc=1207813 |doi=}}</ref> |
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The term ''tension zone'' was first used by K. H. L. Key to describe an area of hybridizing populations that act like a “semipermeable membrane” in terms of gene exchange.<ref>{{Cite journal |last=Key |first=K. H. L. |date=1968 |title=The Concept of Stasipatric Speciation |url=https://www.jstor.org/stable/2412391 |journal=Systematic Zoology |volume=17 |issue=1 |pages=14–22 |doi=10.2307/2412391 |jstor=2412391 |issn=0039-7989}}</ref> This term was later taken by [[Nick Barton|Nicholas Barton]] and [[Godfrey Hewitt]] to denote a hybrid zone maintained by a balance between selection and dispersal.<ref name="Barton_Hewitt" /> Similar models have also previously been termed ''dynamic equilibrium''.<ref name=":0" /><ref>{{Cite journal |last=Bigelow |first=R. S. |date=1965 |title=Hybrid Zones and Reproductive Isolation |url=https://www.jstor.org/stable/2406242 |journal=Evolution |volume=19 |issue=4 |pages=449–458 |doi=10.2307/2406242 |jstor=2406242 |issn=0014-3820}}</ref> |
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A tension zone is characterized by a dispersal-dependent cline (in contrast to a dispersal-independent cline such as a bounded hybrid superiority zone) maintained between the “homogenizing effect” of dispersal and some forces of “spatial heterogeneity”, such as differential selection and introgression.<ref name="Barton_Hewitt" /> Whether a hybrid zone is a tension zone or not is determined by the characteristic scale of selection, ''l'' = σ/√''s'', where σ<sup>2</sup> is dispersal rate and ''s'' is selection strength. The width ''w'' of a dispersal-dependent cline is of the same order as ''l'', whereas a dispersal-independent cline has a much greater ''w'' than ''l''.<ref name="Barton_Hewitt" /> As the hybrids in a tension zone model often exhibit lower fitness compared to the parentals, a “hybrid sink” is maintained through parental gene flow into the tension zone, but rarely hybrid gene flow outwards.<ref name="Barton_Hewitt" /><ref name=":3" /> |
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Certain factors contribute to stability and steepness of hybrid zones within these models by reducing the frequency of inter-population mating and introgression. These include positive assortative mating within populations, habitat selection of different populations and hybrid unfitness. Additionally, it is suggested that individuals in a populations near a tension zone (in which hybrids are less fit), will evolve methods of only mating with their own population to reduce the prevalence of unfit hybrids. This is dubbed reinforcement, and controversy remains as to its importance.<ref>{{cite book |author=D. J. Howard |year=1993 |chapter=Reinforcement: origin, dynamics, and fate of an evolutionary hypothesis |title=Hybrid Zones and the Evolutionary Process |editor=R. G. Harrison |pages=46–69 |location=New York |publisher=[[Oxford University Press]]}}</ref> |
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Although tension zones can be restricted by natural barriers to gene flow, they are generally considered to be environment-independent.<ref name=":1" /> Therefore, the movement of a tension zone can be described independent of ecological characteristics of the habitat. A tension zone can move geographically by mainly three kinds of forces– the fitness variation among individuals of a population, variation in density or dispersal rate, and gene frequencies that may lead to change in density or dispersal.<ref name="Barton_Hewitt" /> |
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=== Mosaic hybrid zone model === |
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A ''mosaic hybrid zone'' is characterized by a “patchy” distribution of genotype frequencies.<ref name=":3" /> Richard Harrison suggested that in some hybrid zones the patterns of environmental heterogeneity can be more complex than can be accounted for by a gradient model, as the transition between two environments may not be a continuous gradient but rather a mosaic distribution comprising patches of varying proportions of the two environments.<ref name=":1" /> A hybrid zone demonstrating a mosaic distribution can be hard to detect. If a transect is taken on a mosaic zone, the distribution of a genotypic trait may present itself as a wave with multiple peaks or plateaus, which may be interpreted as clines depending on the size of the geographical study. The detection of patchy distribution depends on whether the mosaic zone is “fine-grained” or “coarse-grained”,<ref>{{Cite web |date=1968-08-21 |title=Evolution in Changing Environments {{!}} Princeton University Press |url=https://press.princeton.edu/books/paperback/9780691080628/evolution-in-changing-environments |access-date=2024-03-22 |website=press.princeton.edu |language=en}}</ref> i.e. the comparative size of the dispersal distance and the average size of a patch.<ref name=":1" /> |
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=== Primary and secondary hybrid zone === |
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| ⚫ | Hybrid zones can be either ''primary'' or ''secondary''. Primary hybrid zones occur where divergence is taking place between adjacent populations of a previously homogeneous species, possibly leading to [[parapatric speciation]]. As a population spreads across a contiguous area it may spread into an abruptly different environment. Through adaptation to the new environment, the adjacent populations begin parapatric divergence. The point of contact between the older population and the newer population is ideally a stepped cline, but due to dispersal across the line, hybridization takes place and a hybrid zone arises. Secondary hybrid zones in turn arise from secondary contact between two populations that were previously allopatric. In practice it can be quite difficult to distinguish between primary and secondary contact by observing an existing hybrid zone.<ref>{{cite journal |author=J. A. Endler |year=1982 |title=Problems in distinguishing historical from ecological factors in biogeography |journal=[[American Zoologist]] |volume=22 |issue=2 |pages=441–452 |doi=10.1093/icb/22.2.441 |jstor=3882673 |doi-access=free |hdl-access=free |hdl=10536/DRO/DU:30094480}}</ref> Most of the prominent, recognized hybrid zones are thought to be secondary. |
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| ⚫ | One form of hybrid zone results where one species has undergone [[allopatric speciation]] and the two new populations regain contact after a period of geographic isolation. The two populations then mate within an area of contact, producing 'hybrids' which contain a mixture of the alleles distinctive for each population. Thus novel genes flow from either side into the hybrid zone. Genes can also flow back into the distinct populations through interbreeding between hybrids and parental (non-hybrid) individuals ([[introgression]]).<ref>{{cite book |author=Mark Ridley |author-link=Mark Ridley (zoologist) |title=Evolution |publisher=[[Blackwell Publishers]] |year=2003 |isbn=978-1-4051-0345-9 |edition=3rd}}</ref> These processes lead to the formation of a cline between the two pure forms within the hybrid zone. In the centre of such a cline, [[hybrizyme]]s are commonly found. These are alleles that are normally rare in both species but, probably due to [[genetic hitchhiking]] on genes for hybrid fitness, reach high frequencies in the areas where most hybrids are formed.<ref>{{cite journal |author=Schilthuizen M, Hoekstra RF, Gittenberger E |year=1999 |title=Selective increase of a rare haplotype in a land snail hybrid zone |journal=Proceedings of the Royal Society of London B |volume=266 |issue=1434 |pages=2181–2185 |doi=10.1098/rspb.1999.0906 |pmc=1690333}}</ref> |
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== Hybrid zone in conservation biology == |
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Hybrid zones involving a rare species and a more common one can be at risk for [[outbreeding depression]] that reduces the fitness of the rare species. Another risk that can arise is the assimilation of the rare species through loss of rare genotypes or phenotypes.<ref>{{Cite journal |last=Ellstrand |first=Norman C. |date=1992 |title=Gene Flow by Pollen: Implications for Plant Conservation Genetics |url=https://www.jstor.org/stable/3545517 |journal=Oikos |volume=63 |issue=1 |pages=77–86 |doi=10.2307/3545517 |jstor=3545517 |issn=0030-1299}}</ref> This risk is especially high when an [[invasive species]] hybridizes with an endemic species on an island.<ref>{{Cite journal |last1=Levin |first1=Donald A. |last2=Francisco-Ortega |first2=Javier |last3=Jansen |first3=Robert K. |date=1996 |title=Hybridization and the Extinction of Rare Plant Species |url=https://www.jstor.org/stable/2386938 |journal=Conservation Biology |volume=10 |issue=1 |pages=10–16 |doi=10.1046/j.1523-1739.1996.10010010.x |jstor=2386938 |issn=0888-8892}}</ref> However, hybridization can also serve to introduce genetic diversity into small, inbred populations, such as the case with the [[Florida panther]].<ref>{{Cite journal |last=O'Brien |first=S. J. |date=1990-01-01 |title=Genetic introgression within the Florida panther Felis concolor coryi |url=https://nsuworks.nova.edu/cnso_bio_facarticles/1128 |journal=National Geographic Research |volume=6 |issue=4 |pages=485–494}}</ref> In this respect, conservation policies based on taxa instead of genetic structure can be disadvantageous to rare species experiencing inbreeding depression.<ref name=":3" /> |
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Hybrid subpopulations formed through [[Sympatric speciation|sympatric]] or [[parapatric speciation]] at the geographical periphery of larger populations can be important targets for conservation, as they may be sites of future speciation events that lead to higher biodiversity.<ref>{{Cite journal |last1=Lesica |first1=Peter |last2=Allendorf |first2=Fred W. |date=1995 |title=When Are Peripheral Populations Valuable for Conservation? |url=https://www.jstor.org/stable/2386984 |journal=Conservation Biology |volume=9 |issue=4 |pages=753–760 |doi=10.1046/j.1523-1739.1995.09040753.x |jstor=2386984 |issn=0888-8892}}</ref> |
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Hybrid zones can be a good indicator in the study of [[climate change]]. Monitoring the range of hybrid zones through genetic methods such as geographical cline analysis of genotype distribution can tell us the populations’ response to historical as well as ongoing changing environments.<ref name=":5">{{Cite journal |last1=Taylor |first1=Scott A. |last2=Larson |first2=Erica L. |last3=Harrison |first3=Richard G. |date=2015-05-13 |title=Hybrid zones: windows on climate change |url=http://dx.doi.org/10.1016/j.tree.2015.04.010 |journal=Trends in Ecology & Evolution |volume=30 |issue=7 |pages=398–406 |doi=10.1016/j.tree.2015.04.010 |pmid=25982153 |issn=0169-5347|pmc=4794265 }}</ref> Examining the exchange of adaptive alleles or genomic regions can also be useful in mapping the populations’ adaptation to climatic niches.<ref name=":5" /> |
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== Case studies == |
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=== Marine hybrid zone: blue mussels === |
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[[File:Blue mussel clump.jpg|thumb|''[[Mytilus edulis]]'']] |
[[File:Blue mussel clump.jpg|thumb|''[[Mytilus edulis]]'']] |
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| ⚫ | Hybrid zones are thought to be less common in marine than terrestrial environments. However, [[blue mussel]] populations show extensive hybridisation worldwide and are a well studied example of a marine hybrid zone. There are multiple sites of hybridisation between the closely related species ''[[Mytilus edulis]]'', ''[[Mytilus |
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| ⚫ | Hybrid zones are thought to be less common in marine than terrestrial environments. However, [[blue mussel]] populations show extensive hybridisation worldwide and are a well studied example of a marine hybrid zone. There are multiple sites of hybridisation between the closely related species ''[[Mytilus edulis]]'', ''[[Mytilus trossulus]]'' and ''[[Mytilus galloprovincialis]]'' across the [[North Atlantic]] and [[Pacific]] coasts. These hybrid zones vary considerably. Some hybrid zones, such as the one in [[Newfoundland and Labrador|Newfoundland]] in [[Canada]] show remarkably few hybrids, while in the [[Baltic Sea]] most individuals are hybrids. |
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*The genus ''[[Mytilus (genus)|Mytilus]]'' is at one point restricted to the North Pacific but spreads to the Atlantic through the Bering Strait around {{Ma|3.5}}.<ref>{{cite journal |author=G .J. Vermeij |year=1991 |title=Anatomy of an invasion: the trans-Arctic interchange |journal=[[Paleobiology (journal)|Paleobiology]] |volume=17 |issue=3 |pages=281–307 |jstor=2400870 |doi=}}</ref> |
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*The genus ''[[Mytilus (bivalve)|Mytilus]]'' is at one point restricted to the North Pacific but spreads to the Atlantic through the Bering Strait around {{Ma|3.5}}.<ref>{{cite journal |author=G. J. Vermeij |year=1991 |title=Anatomy of an invasion: the trans-Arctic interchange |journal=[[Paleobiology (journal)|Paleobiology]] |volume=17 |issue=3 |pages=281–307 |jstor=2400870 |doi=10.1017/S0094837300010617|bibcode=1991Pbio...17..281V |s2cid=87924250 }}</ref> |
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*Recently, in post-glacial times, ''M. trossulus'' from the Pacific enters the Atlantic and colonises shores on both sides, and meets with the local ''M. edulis''.<ref name="Riginos">{{cite journal |author1=C. Riginos |author2=C. W. Cunningham |year=2005 |title=Local adaptation and species segregation in two mussel (''Mytilus edulis'' × ''Mytilus trossulus'') hybrid zones |journal=[[Molecular Ecology]] |volume=14 |issue=2 |pages=381–400 |doi=10.1111/j.1365-294X.2004.02379.x |pmid=15660932 |url=http://www.biology.duke.edu/cunningham/pdfs/Riginos.Cunningham.Mol.Ecol.2005.pdf |doi-access=free }}</ref> |
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The Canadian mussel hybrid zone is unusual because both species are found along the entire shore (a [[mosaic]] pattern) instead of the typical cline found in most hybrid zones. Studies of [[mtDNA]] and [[allozyme]]s in adult populations show that the distribution of genotypes between the two species is bimodal; pure parental types are most common (representing above 75% of individuals) while [[backcross]]es close to parental forms are the next most prevalent. F1 hybrid crosses represent less than 2.5% of individuals.<ref>{{cite journal | |
The Canadian mussel hybrid zone is unusual because both species are found along the entire shore (a [[mosaic]] pattern) instead of the typical cline found in most hybrid zones. Studies of [[mtDNA]] and [[allozyme]]s in adult populations show that the distribution of genotypes between the two species is bimodal; pure parental types are most common (representing above 75% of individuals) while [[backcross]]es close to parental forms are the next most prevalent. F1 hybrid crosses represent less than 2.5% of individuals.<ref>{{cite journal |author1=Carlos Saavedra |author2=Donald T. Stewart |author3=Rebecca R. Stanwood |author4=Eleftherios Zouros |year=1996 |title=Species-specific segregation of gender-associated mitochondrial DNA types in an area where two mussel species (''Mytilus edulis'' and ''M. trossulus'') hybridize |journal=[[Genetics (journal)|Genetics]] |volume=143 |issue=3 |pages=1359–1367 |doi=10.1093/genetics/143.3.1359 |pmid=8807307 |pmc=1207404 |url=http://www.genetics.org/content/143/3/1359.full.pdf }}</ref> |
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The low frequency of F1 hybrids coupled with some introgression allows us to infer that although fertile hybrids can be produced, significant reproductive barriers exist and the two species are sufficiently deviated that they are now able to avoid recombinational collapse despite habitat sharing. One reason that could account for keeping taxa separate through prezygotic isolation is that in this region ''M. edulis'' spawns over a narrow 2–3 week period in July, while ''M. trossulus'' spawned over a more extensive period between late spring to early autumn.<ref name="Toro">{{cite journal | |
The low frequency of F1 hybrids coupled with some introgression allows us to infer that although fertile hybrids can be produced, significant reproductive barriers exist and the two species are sufficiently deviated that they are now able to avoid recombinational collapse despite habitat sharing. One reason that could account for keeping taxa separate through prezygotic isolation is that in this region ''M. edulis'' spawns over a narrow 2–3 week period in July, while ''M. trossulus'' spawned over a more extensive period between late spring to early autumn.<ref name="Toro">{{cite journal |author1=J. E. Toro |author2=R. J. Thompson |author3=D. J. Innes |year=2002 |title=Reproductive isolation and reproductive output in two sympatric mussel species (''Mytilus edulis'', ''M. trossulus'') and their hybrids from Newfoundland |journal=[[Marine Biology (journal)|Marine Biology]] |volume=141 |issue=5 |pages=897–909 |url=https://www.mun.ca/biology/dinnes/Reproduction.pdf |doi=10.1007/s00227-002-0897-3|bibcode=2002MarBi.141..897T |s2cid=52028915 }}</ref> No [[infertile|infertility]] or developmental retardation was found in the hybrid individuals, allowing them to introgress with pure species.<ref name="Toro"/> |
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==See also== |
==See also== |
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| Line 36: | Line 61: | ||
* [[Hybrid swarm]] |
* [[Hybrid swarm]] |
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* [[Hybrid speciation]] |
* [[Hybrid speciation]] |
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* [[Reproductive isolation|Species boundary]] |
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* [[Introgression]] |
* [[Introgression]] |
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* [[Hybrizyme]] |
* [[Hybrizyme]] |
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* [[Syngameon]] |
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== References == |
== References == |
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Latest revision as of 01:43, 22 November 2024
A hybrid zone exists where the ranges of two interbreeding species or diverged intraspecific lineages meet and cross-fertilize. Hybrid zones can form in situ due to the evolution of a new lineage[1][page needed] but generally they result from secondary contact of the parental forms after a period of geographic isolation, which allowed their differentiation. Hybrid zones are useful in studying the genetics of speciation as they can provide natural examples of differentiation and gene flow between populations that are at some point on the continuum between diverging populations and separate species with reproductive isolation.
Definition
[edit]Hybrid zones are areas where the hybrid offspring of two divergent taxa (species, subspecies or genetic "forms") are prevalent and there is a cline in the genetic composition of populations from one taxon to the other.[2] The two (or more) genetically differentiated species or lineages contributing to formation of a hybrid zone are regarded as parental forms. Precise definitions of hybrid zones vary; some insist on increased variability of fitness within the zone, others that hybrids be identifiably different from parental forms and others that they represent secondary contact alone.[3] The widths of such zones can vary from tens of metres to hundreds of kilometres.[4] The shape of the zones (clines) can be gradual or stepped.[2] Additionally, hybrid zones may be ephemeral or long-lasting.[5]
Some hybrid zones can be seen as presenting a paradox for the biological definition of a species, usually given as "a population of actually or potentially interbreeding individuals that produce fertile offspring" [6] under what has become known as the Biological Species Concept. Under this definition, both parental forms could be argued to be the same species if they produce fertile offspring at least some of the time. However, the two parental populations or species often remain identifiably distinct, conforming to an alternative, and presently preferred concept of species as "taxa that retain their identity despite gene flow".[7][2]
The clines of hybrid zones can be observed by recording the frequency of certain diagnostic alleles or phenotypic characteristics for either population along a transect between the two parental populations or species. Often the clines take the form of a sigmoidal curve. They can be wide (gradual) or narrow (steep) depending on the ratio of hybrid survival to recombination of genes.[8] Hybrid zones which show no regular transition from one taxon to the other, but rather a patchy distribution of parental forms and subpopulations with hybrid background, are termed mosaic hybrid zones.[5]
Models and theories
[edit]Various models and theories have been developed by the researchers of hybrid zones. Major models can be largely categorized into four types: ephemeral hybrid zone theory,[9] bounded hybrid superiority model,[9] mosaic hybrid zone model[5] and tension zone model.[2] In each model, different evolutionary forces are attributed different levels of importance. The different models result largely from the study of different biological material (natural populations). The four major models operate mostly under a general framework of either a balance between natural selection and dispersal or interaction between genotypes and environment.[10] Different hybrid zones may fit different models and no single theory or model serves to explain all the hybrid zones found in nature.
Ephemeral hybrid zone theory
[edit]Some early evolutionary biologists who preferred a biological species concept, such as Ernst Mayr[11] and Theodosius Dobzhansky,[12] believed that hybrid zones are generally rare and ephemeral, with an eventual fate of either merging of the hybridizing populations or reinforcement, which leads to a speciation event. The extinction of one of the hybridizing populations through introgression is sometimes termed “waves of advance”.[13] (Although this term can also refer to the spreading of advantageous allele across a reproductive barrier[14]) The ephemerality of hybrid zone has been countered by the discovery of many hybrid zones that has lasted for a long period of time,[9] up to 100,000 years found between the iguanid lizards, Sceloporus woodi and S. undulatus undulatus.[15]
Bounded hybrid superiority
[edit]The bounded hybrid superiority model predicts that hybrids have higher fitness in a habitat that is intermediate between those of their parental populations.[9] The hybrid habitat occurs usually, but not necessarily, on a narrow ecotone. Clines of a bounded hybrid superiority zone reflect a smooth gradient corresponding to the gradient of differential selection strength in fitness-related characteristics.[2] The bounded superiority model places a high importance on the ecological aspect of the habitat. In fact, botanist Edgar Anderson suggested that hybrid populations are more likely to inhabit ecologically disturbed areas, which often occur under human’s modification of landscapes or geological events that create novel habitat conditions.[2] He argued that hybrid zones are essentially formed via “hybridization of habitats”.[16] Anderson also considered natural hybridization as a positive evolutionary stimulus that allows different populations and lineages to exchange adaptive genetic elements[17]—similar view that place a high evolutionary importance on hybrid zones is more prevalent among botanists, in contrast to zoologists who are more likely see hybrid zones as more of a “natural laboratory” of population genetics.[13] Some criticism for the bounded superiority model suggests that hybrid zones with higher hybrid fitness are theoretically unlikely to be distributed along narrow ecotones;[18] some also point out that there has not been direct empirical evidence of higher hybrid fitness along an ecological gradient (i.e. ecotones).[5]
Tension zone model
[edit]The term tension zone was first used by K. H. L. Key to describe an area of hybridizing populations that act like a “semipermeable membrane” in terms of gene exchange.[19] This term was later taken by Nicholas Barton and Godfrey Hewitt to denote a hybrid zone maintained by a balance between selection and dispersal.[2] Similar models have also previously been termed dynamic equilibrium.[9][20]
A tension zone is characterized by a dispersal-dependent cline (in contrast to a dispersal-independent cline such as a bounded hybrid superiority zone) maintained between the “homogenizing effect” of dispersal and some forces of “spatial heterogeneity”, such as differential selection and introgression.[2] Whether a hybrid zone is a tension zone or not is determined by the characteristic scale of selection, l = σ/√s, where σ2 is dispersal rate and s is selection strength. The width w of a dispersal-dependent cline is of the same order as l, whereas a dispersal-independent cline has a much greater w than l.[2] As the hybrids in a tension zone model often exhibit lower fitness compared to the parentals, a “hybrid sink” is maintained through parental gene flow into the tension zone, but rarely hybrid gene flow outwards.[2][10]
Although tension zones can be restricted by natural barriers to gene flow, they are generally considered to be environment-independent.[5] Therefore, the movement of a tension zone can be described independent of ecological characteristics of the habitat. A tension zone can move geographically by mainly three kinds of forces– the fitness variation among individuals of a population, variation in density or dispersal rate, and gene frequencies that may lead to change in density or dispersal.[2]
Mosaic hybrid zone model
[edit]A mosaic hybrid zone is characterized by a “patchy” distribution of genotype frequencies.[10] Richard Harrison suggested that in some hybrid zones the patterns of environmental heterogeneity can be more complex than can be accounted for by a gradient model, as the transition between two environments may not be a continuous gradient but rather a mosaic distribution comprising patches of varying proportions of the two environments.[5] A hybrid zone demonstrating a mosaic distribution can be hard to detect. If a transect is taken on a mosaic zone, the distribution of a genotypic trait may present itself as a wave with multiple peaks or plateaus, which may be interpreted as clines depending on the size of the geographical study. The detection of patchy distribution depends on whether the mosaic zone is “fine-grained” or “coarse-grained”,[21] i.e. the comparative size of the dispersal distance and the average size of a patch.[5]
Primary and secondary hybrid zone
[edit]Hybrid zones can be either primary or secondary. Primary hybrid zones occur where divergence is taking place between adjacent populations of a previously homogeneous species, possibly leading to parapatric speciation. As a population spreads across a contiguous area it may spread into an abruptly different environment. Through adaptation to the new environment, the adjacent populations begin parapatric divergence. The point of contact between the older population and the newer population is ideally a stepped cline, but due to dispersal across the line, hybridization takes place and a hybrid zone arises. Secondary hybrid zones in turn arise from secondary contact between two populations that were previously allopatric. In practice it can be quite difficult to distinguish between primary and secondary contact by observing an existing hybrid zone.[22] Most of the prominent, recognized hybrid zones are thought to be secondary.
One form of hybrid zone results where one species has undergone allopatric speciation and the two new populations regain contact after a period of geographic isolation. The two populations then mate within an area of contact, producing 'hybrids' which contain a mixture of the alleles distinctive for each population. Thus novel genes flow from either side into the hybrid zone. Genes can also flow back into the distinct populations through interbreeding between hybrids and parental (non-hybrid) individuals (introgression).[23] These processes lead to the formation of a cline between the two pure forms within the hybrid zone. In the centre of such a cline, hybrizymes are commonly found. These are alleles that are normally rare in both species but, probably due to genetic hitchhiking on genes for hybrid fitness, reach high frequencies in the areas where most hybrids are formed.[24]
Hybrid zone in conservation biology
[edit]Hybrid zones involving a rare species and a more common one can be at risk for outbreeding depression that reduces the fitness of the rare species. Another risk that can arise is the assimilation of the rare species through loss of rare genotypes or phenotypes.[25] This risk is especially high when an invasive species hybridizes with an endemic species on an island.[26] However, hybridization can also serve to introduce genetic diversity into small, inbred populations, such as the case with the Florida panther.[27] In this respect, conservation policies based on taxa instead of genetic structure can be disadvantageous to rare species experiencing inbreeding depression.[10]
Hybrid subpopulations formed through sympatric or parapatric speciation at the geographical periphery of larger populations can be important targets for conservation, as they may be sites of future speciation events that lead to higher biodiversity.[28]
Hybrid zones can be a good indicator in the study of climate change. Monitoring the range of hybrid zones through genetic methods such as geographical cline analysis of genotype distribution can tell us the populations’ response to historical as well as ongoing changing environments.[29] Examining the exchange of adaptive alleles or genomic regions can also be useful in mapping the populations’ adaptation to climatic niches.[29]
Case studies
[edit]Marine hybrid zone: blue mussels
[edit]
Hybrid zones are thought to be less common in marine than terrestrial environments. However, blue mussel populations show extensive hybridisation worldwide and are a well studied example of a marine hybrid zone. There are multiple sites of hybridisation between the closely related species Mytilus edulis, Mytilus trossulus and Mytilus galloprovincialis across the North Atlantic and Pacific coasts. These hybrid zones vary considerably. Some hybrid zones, such as the one in Newfoundland in Canada show remarkably few hybrids, while in the Baltic Sea most individuals are hybrids.
Based on the fossil record and genetic marker studies the following chronology is used to explain the Canadian mussel hybrid zone:
- The genus Mytilus is at one point restricted to the North Pacific but spreads to the Atlantic through the Bering Strait around 3.5 million years ago.[30]
- M. trossulus evolves in the North Pacific and M. edulis in the Atlantic in near allopatry as migration across the Bering Strait is very low.
- Recently, in post-glacial times, M. trossulus from the Pacific enters the Atlantic and colonises shores on both sides, and meets with the local M. edulis.[31]
The Canadian mussel hybrid zone is unusual because both species are found along the entire shore (a mosaic pattern) instead of the typical cline found in most hybrid zones. Studies of mtDNA and allozymes in adult populations show that the distribution of genotypes between the two species is bimodal; pure parental types are most common (representing above 75% of individuals) while backcrosses close to parental forms are the next most prevalent. F1 hybrid crosses represent less than 2.5% of individuals.[32]
The low frequency of F1 hybrids coupled with some introgression allows us to infer that although fertile hybrids can be produced, significant reproductive barriers exist and the two species are sufficiently deviated that they are now able to avoid recombinational collapse despite habitat sharing. One reason that could account for keeping taxa separate through prezygotic isolation is that in this region M. edulis spawns over a narrow 2–3 week period in July, while M. trossulus spawned over a more extensive period between late spring to early autumn.[33] No infertility or developmental retardation was found in the hybrid individuals, allowing them to introgress with pure species.[33]
See also
[edit]References
[edit]- ^ Endler, J. (1977). Geographic Variation, Speciation and Clines. Monographs in Population Biology. Vol. 10. Princeton, NJ: Princeton University Press. pp. 1–246. ISBN 9780691081922. PMID 409931.
- ^ a b c d e f g h i j k N. H. Barton & G. M. Hewitt (1985). "Analysis of hybrid zones". Annual Review of Ecology and Systematics. 16: 113–148. doi:10.1146/annurev.es.16.110185.000553.
- ^ Murray, 1985[citation needed]
- ^ Morgan-Richards, Mary; Wallis, Graham P. (2003). "A comparison of five hybrid zones of the weta Hemideina thoracica (Orthoptera: Anostostomatidae): degree of cytogenetic differentiation fails to predict zone width". Evolution. 57 (4): 849–861. doi:10.1111/j.0014-3820.2003.tb00296.x. ISSN 0014-3820. PMID 12778554.
- ^ a b c d e f g Harrison, Richard (1990). "Hybrid zones: windows on evolutionary process". Oxford Surveys in Evolutionary Biology. 7.
- ^ Ernst Mayr (1942). Systematics and the Origin of Species. New York: Columbia University Press.
- ^ Mallet, James (1995-07-01). "A species definition for the modern synthesis". Trends in Ecology & Evolution. 10 (7): 294–299. doi:10.1016/0169-5347(95)90031-4. ISSN 0169-5347. PMID 21237047.
- ^ N. H. Barton (1983). "Multilocus clines". Evolution. 37 (3): 454–471. doi:10.2307/2408260. JSTOR 2408260. PMID 28563316.
- ^ a b c d e William S. Moore (1977). "An evaluation of narrow hybrid zones in vertebrates". Quarterly Review of Biology. 52 (3): 263–278. doi:10.1086/409995. JSTOR 2824163. S2CID 14462807.
- ^ a b c d Arnold, Michael L. (1997). Natural hybridization and evolution. Oxford series in ecology and evolution. New York Oxford: Oxford University Press. ISBN 978-0-19-509974-4.
- ^ Mayr, Ernst (1999). Systematics and the Origin of Species, from the Viewpoint of a Zoologist. Harvard University Press. ISBN 978-0-674-86250-0.
- ^ "Speciation as a Stage in Evolutionary Divergence". The American Naturalist. 74 (753): 312–321. July 1940. doi:10.1086/280899. ISSN 0003-0147.
- ^ a b Harrison, Richard G (1993-06-17), "Hybrids and Hybrid Zones: Historical Perspective", Hybrid Zones and the Evolutionary Process, Oxford University PressNew York, NY, pp. 3–12, doi:10.1093/oso/9780195069174.003.0001, ISBN 978-0-19-506917-4, retrieved 2024-03-22
- ^ FISHER, R. A. (June 1937). "The Wave of Advance of Advantageous Genes". Annals of Eugenics. 7 (4): 355–369. doi:10.1111/j.1469-1809.1937.tb02153.x. hdl:2440/15125. ISSN 2050-1420.
- ^ Jackson, James F. (1973-03-01). "The Phenetics and Ecology of a Narrow Hybrid Zone". Evolution. 27 (1): 58–68. doi:10.1111/j.1558-5646.1973.tb05917.x. ISSN 0014-3820. PMID 28563661.
- ^ Anderson, Edgar (1948). "Hybridization of the Habitat". Evolution. 2 (1): 1–9. doi:10.2307/2405610. ISSN 0014-3820. JSTOR 2405610.
- ^ Anderson, E.; Stebbins, G. L. (1954). "Hybridization as an Evolutionary Stimulus". Evolution. 8 (4): 378–388. doi:10.2307/2405784. ISSN 0014-3820. JSTOR 2405784.
- ^ Barton, N. H.; Hewitt, G. M. (1985). "Analysis of Hybrid Zones". Annual Review of Ecology and Systematics. 16: 113–148. doi:10.1146/annurev.es.16.110185.000553. ISSN 0066-4162. JSTOR 2097045.
- ^ Key, K. H. L. (1968). "The Concept of Stasipatric Speciation". Systematic Zoology. 17 (1): 14–22. doi:10.2307/2412391. ISSN 0039-7989. JSTOR 2412391.
- ^ Bigelow, R. S. (1965). "Hybrid Zones and Reproductive Isolation". Evolution. 19 (4): 449–458. doi:10.2307/2406242. ISSN 0014-3820. JSTOR 2406242.
- ^ "Evolution in Changing Environments | Princeton University Press". press.princeton.edu. 1968-08-21. Retrieved 2024-03-22.
- ^ J. A. Endler (1982). "Problems in distinguishing historical from ecological factors in biogeography". American Zoologist. 22 (2): 441–452. doi:10.1093/icb/22.2.441. hdl:10536/DRO/DU:30094480. JSTOR 3882673.
- ^ Mark Ridley (2003). Evolution (3rd ed.). Blackwell Publishers. ISBN 978-1-4051-0345-9.
- ^ Schilthuizen M, Hoekstra RF, Gittenberger E (1999). "Selective increase of a rare haplotype in a land snail hybrid zone". Proceedings of the Royal Society of London B. 266 (1434): 2181–2185. doi:10.1098/rspb.1999.0906. PMC 1690333.
{{cite journal}}: CS1 maint: multiple names: authors list (link) - ^ Ellstrand, Norman C. (1992). "Gene Flow by Pollen: Implications for Plant Conservation Genetics". Oikos. 63 (1): 77–86. doi:10.2307/3545517. ISSN 0030-1299. JSTOR 3545517.
- ^ Levin, Donald A.; Francisco-Ortega, Javier; Jansen, Robert K. (1996). "Hybridization and the Extinction of Rare Plant Species". Conservation Biology. 10 (1): 10–16. doi:10.1046/j.1523-1739.1996.10010010.x. ISSN 0888-8892. JSTOR 2386938.
- ^ O'Brien, S. J. (1990-01-01). "Genetic introgression within the Florida panther Felis concolor coryi". National Geographic Research. 6 (4): 485–494.
- ^ Lesica, Peter; Allendorf, Fred W. (1995). "When Are Peripheral Populations Valuable for Conservation?". Conservation Biology. 9 (4): 753–760. doi:10.1046/j.1523-1739.1995.09040753.x. ISSN 0888-8892. JSTOR 2386984.
- ^ a b Taylor, Scott A.; Larson, Erica L.; Harrison, Richard G. (2015-05-13). "Hybrid zones: windows on climate change". Trends in Ecology & Evolution. 30 (7): 398–406. doi:10.1016/j.tree.2015.04.010. ISSN 0169-5347. PMC 4794265. PMID 25982153.
- ^ G. J. Vermeij (1991). "Anatomy of an invasion: the trans-Arctic interchange". Paleobiology. 17 (3): 281–307. Bibcode:1991Pbio...17..281V. doi:10.1017/S0094837300010617. JSTOR 2400870. S2CID 87924250.
- ^ C. Riginos; C. W. Cunningham (2005). "Local adaptation and species segregation in two mussel (Mytilus edulis × Mytilus trossulus) hybrid zones" (PDF). Molecular Ecology. 14 (2): 381–400. doi:10.1111/j.1365-294X.2004.02379.x. PMID 15660932.
- ^ Carlos Saavedra; Donald T. Stewart; Rebecca R. Stanwood; Eleftherios Zouros (1996). "Species-specific segregation of gender-associated mitochondrial DNA types in an area where two mussel species (Mytilus edulis and M. trossulus) hybridize" (PDF). Genetics. 143 (3): 1359–1367. doi:10.1093/genetics/143.3.1359. PMC 1207404. PMID 8807307.
- ^ a b J. E. Toro; R. J. Thompson; D. J. Innes (2002). "Reproductive isolation and reproductive output in two sympatric mussel species (Mytilus edulis, M. trossulus) and their hybrids from Newfoundland" (PDF). Marine Biology. 141 (5): 897–909. Bibcode:2002MarBi.141..897T. doi:10.1007/s00227-002-0897-3. S2CID 52028915.