Evidence for speciation by reinforcement

File:Brown Tree Frog 2.jpg, Litoria ewingi]]

The two frog species Litoria ewingi and L. verreauxii live in southern Australia with their two ranges overlapping. The species have very similar calls in allopatry, but express clinal variation in sympatry, with notable distinctness in calls that generate female preference discrimination. The zone of overlap sometimes forms hybrids and is thought to originate by secondary contact of once fully allopatric populations.

Allopatric populations of Gastrophryne olivacea and G. carolinensis have recently come into secondary contact due to forest clearing. The calls that the males make to attract females differ significantly in frequency and duration in the area where the two species overlap, despite them having similar calls where they do not.{{rp|359}} Further, the hybrids that form in sympatry have calls that are intermediate between the two. Similar patterns of reproductive character displacement involving acoustic displays have been found in Hyla cinerea and H. gratiosa, with greater female preference for conspecific males in areas of sympatry.{{Citation |title=Reproductive character displacement in the acoustic communication system of green tree frogs (Hyla cinerea)| author=Gerlinde Höbel and H. Carl Gerhardt | journal=Evolution | year=2003 | volume=57 | issue=4 | pages=894–904 | doi=10.1554/0014-3820(2003)057[0894:RCDITA]2.0.CO;2 | pmid=12778558| s2cid=198155155 }}

Three species of true frogs (Lithobates sphenocephalus, L. berlandieri, and L. blairi) are temporally isolated in that their breeding seasons are spaced out in areas where they live in sympatry, but not where they live in allopatry.{{Citation |title=Premating Isolating Mechanisms Among Three Species of the Rana pipiens Complex in Texas and Southern Oklahoma | author=David M. Hillis | journal=Copeia | year=1981 | volume=1981 | issue=2 | pages=312–319 | doi= 10.2307/1444220| jstor=1444220 }} Selection against interspecific mating due to low hybrid fitness and low hybrid fertility has reinforced the observed character displacement of breeding times.

The rainforests of northeast Queensland, Australia were separated into north and south refugia by climate fluctuations of the Pliocene and Pleistocene.{{Citation |title=Comparative phylogeography and the history of endemic vertebrates in the Wet Tropics rainforests of Australia | author=C. J. Schneider, M. Cunningham, and C. Moritz | journal=Molecular Ecology | year=1998 | volume=7 | issue=4 | pages=487–498 | doi=10.1046/j.1365-294x.1998.00334.x | s2cid=84601584 | doi-access=free | bibcode=1998MolEc...7..487S }} About 6500 years ago, the rainforests reconnected, bringing the diverged, incipient populations of Litoria genimaculata into secondary contact. The species contact zones exhibit, "strong postzygotic selection against hybrids" and enhanced isolation from differences in mating call.{{Citation |title=Reinforcement drives rapid allopatric speciation | author=Conrad J. Hoskin, Megan Higgie, Keith R. McDonald, and Craig Moritz | journal=Nature | year=2005 | volume=437 | issue= 7063| pages=1353–1356 | doi=10.1038/nature04004 | pmid=16251964| bibcode=2005Natur.437.1353H | s2cid=4417281 }}

An alternative to detecting reproductive character displacement in populations that overlap in sympatry is measuring rates of hybridization in contact zones. The frog species Anaxyrus americanus and Anaxyrus woodhousii have shown a decrease in hybridization from 9% to 0% over approximately 30 years.{{Citation |title=Effects of thirty years hybridization on the toads Bufo americanus and Bufo woodhousii fowleri at Bloomington, Indian | author=J. Michael Jones | journal=Evolution | year=1973 | volume=27 | issue=3 | pages=435–448 | doi=10.1111/j.1558-5646.1973.tb00690.x | pmid=28564913 | s2cid=39042605 | doi-access=free }} A similar pattern was detected in the sympatric spadefoot toads Spea multiplicata and S. bombifrons have hybridized with decreasing frequency over a 27-year period (about 13 generations).{{Citation |title=A test of alternative hypotheses for the evolution of reproductive isolation between spadefoot toads: Support for the reinforcement hypothesis | author=Karin S. Pfennig | journal=Evolution | year=2003 | volume=57 | issue=12 | pages=2842–2851 | doi=10.1554/03-228 | pmid=14761062| s2cid=198152266 }}

File:Geospiza fuliginosa.jpg, one of Darwin's finches of the Galápagos]]

The Ficedula flycatchers exhibit a pattern that suggests premating isolation is being reinforced by sexual selection.{{Citation |title=A sexually selected character displacement in flycatchers reinforces premating isolation | author=Glenn-Peter Sætre, T. Moum, S. Bures, M. Kral, M. Adamjan, and J. Moreno | journal=Nature | year=1997 | volume=387 | issue= 6633| pages=589–592 | doi=10.1038/42451 | bibcode=1997Natur.387..589S | s2cid=4363912 }} The pied flycatcher (Ficedula hypoleuca) has brown females, brown males, and black-and-white males. The related collard flycatcher (Ficedula albicollis) has brown females and only black-and-white males. The two species exist in separate populations that overlap in a zone of sympatry. In the range of overlap, only brown males of F. hypoleuca exist and are thought to have evolved the brown plumage to prevent hybridization,{{Citation |title=Hybridization and breeding success of collared and pied flycatchers on the island of Gotland | author=R. V. Alatalo, L. Gustafsson, and A. Lundberg | journal=Auk | year=1982 | volume=99 | pages=285–291 }} though there is also evidence indicating that such character displacement is explained by heterospecific competition for territory rather than reinforcement.{{Cite journal|last1=Vallin|first1=Niclas|last2=Rice|first2=Amber M.|last3=Bailey|first3=Richard I.|last4=Husby|first4=Arild|last5=Qvarnström|first5=Anna|title=Positive Feedback Between Ecological and Reproductive Character Displacement in a Young Avian Hybrid Zone |date=April 2012|journal=Evolution|language=en|volume=66|issue=4|pages=1167–1179|doi=10.1111/j.1558-5646.2011.01518.x|pmid=22486696 |s2cid=13238049 |doi-access=free}} Mating choice tests of the species find that females of both species choose conspecific males in sympatry, but heterospecific males in allopatry (see conspecific song preference). The patterns could suggest mimicry, driven by interspecific competition;{{rp|361}} however, song divergence has been detected that shows a similar pattern to the mating preferences.{{Citation |title=Divergent character displacement in the song of two allospecies: the pied flycatcher Ficedula hypoleuca and the collared flycatcher Ficedula albicollis | author=Lars Wallin | journal=Ibis | year=1986 | volume=128 | issue= 2| pages=251–259 | doi= 10.1111/j.1474-919X.1986.tb02672.x }}

Geospiza fuliginosa and G. difficilis males on the Galápagos Islands show a noted preference for conspecific females where they meet in sympatry, but not in allopatry.{{Citation |title=Species recognition in Darwin's finches (Geospiza, Gould). II. Geographic variation in mate preference | author=L. M. Ratcliffe and Peter R. Grant | journal=Animal Behaviour | year=1983 | volume=31 | issue= 4| pages=1154–1165 | doi= 10.1016/S0003-3472(83)80022-0| s2cid=53178974 }} Other birds such as the dark and light subspecies of the western grebe show enhanced prezygotic isolation.J. T. Ratti (1979). Reproductive Separation and Isolating Mechanisms between Sympatric Dark- and Light- Phase Western Grebes. American Ornithological Society, 93(3), 573–586. It has been argued that reinforcement is extremely common in birds and has been documented in a wide range of bird species.{{Citation |title=Pervasive Reinforcement and the Role of Sexual Selection in Biological Speciation |author=Emily J. Husdon and Trevor D. Price |journal=Journal of Heredity |year=2014 |volume=105 |pages=821–833 |doi=10.1093/jhered/esu041 |pmid=25149257 |doi-access=free }}

Reproductive character displacement in body size was detected in sympatric populations of Orconectes rusticus and O. sanbornii.{{Citation |title=Evaluation of Possible Reproductively Mediated Character Displacement in the Crayfishes, Orconectes rusticus and O. sanbornii | author=Mark J. Butler IV | journal=Ohio Journal of Science | year=1988 | volume=88 | issue=3 | pages=87–91 }}

An example of gametic isolation involves the allopatric sea urchins (Arbacia) have minimal bindin differences (bindin is a protein involved in the process of sea urchin fertilization, used for species-specific recognition of the egg by the sperm) and have insufficient barriers to fertilization.{{rp|243}} Comparison with the sympatric species Echinometra and Strongylocentrotus of the Indo-Pacific finds that they have significant differences in bindin proteins for fertilization and marked fertilization barriers.{{Citation |title=Mitochondrial DNA and Bindin Gene Sequence Evolution Among Allopatric Species of the Sea Urchin Genus Arbacia | author=Edward C. Metz, Gerardo Gómez-Gutiérrez, and Victor D. Vacquier | journal=Molecular Biology and Evolution | year=1998 | volume=15 | issue=2 | pages=185–195 | doi=10.1093/oxfordjournals.molbev.a025914 | pmid=9491615 | doi-access=free }}

File:Echinometra viridis (Reef Urchin).jpg, one of several species in the genus that produce fertile hybrids]]

Laboratory matings of closely related sea urchin species Echinometra oblonga and E. sp. C (the species is unnamed, dubbed C) produce fertile and viable hybrids, but are unable to fertilize eggs of the parent species due to divergence of the alleles that code for bindin proteins: an example of post-zygotic isolation.{{rp|343–344}} Populations in sympatry manifest this difference in bindin protein versus those in allopatry.{{rp|343–344}} Selection actively acts against the formation of hybrids in both nature (as no documented cases of hybrids have been found) and in the laboratory.{{Citation |title=Reproductive character displacement and the genetics of gamete recognition in tropical sea urchins | author=Laura B. Geyer and Stephen R. Palumbi | journal=Evolution | year=2003 | volume=57 | issue=5 | pages=1049–1060 | doi=10.1554/0014-3820(2003)057[1049:RCDATG]2.0.CO;2 | pmid=12836822 | s2cid=198154301 }} Here, the evolution of female egg receptors is thought to pressure bindin evolution in a selective runaway process. This example of reproductive character displacement is highly suggestive of being the result of—and has been cited as strong evidence for—reinforcement.{{rp|343–344}}

In British Columbia, benthic and limnetic morphs of Gasterosteus aculeatus exist together in sympatry in some lakes, while containing only one morph in other lakes.{{Citation |title=Reinforcement of stickleback mate preferences: Sympatry breeds contempt | author=Howard D. Rundle | journal=Dolph Schluter | year=1998 | volume=52 | issue=1 | pages=200–208 | doi=10.1111/j.1558-5646.1998.tb05153.x | pmid=28568163 | hdl=2429/6366 | s2cid=40648544 | hdl-access=free }} Female benthic morphs in sympatric populations actively discriminate against limnetic males, resulting in low rates of crossing (some gene flow has occurred between the morphs) and low fitness hybrids.{{rp|360}} Both selection against hybrids and reproductive character displacement in egg fertilization is observed in Etheostoma lepidum and E. spectabile.{{Citation |title=Duration of sperm function in the percid fishes Etheostoma lepidum and Etheostoma spectabile, associated with sympatry of the parent populations | author=C. Hubbs | journal=Copeia | year=1960 | volume=1960 | issue=1 | pages=1–8 | doi= 10.2307/1439836| jstor=1439836 }}

A strong case of reinforcement occurring in fungi comes from studies of Neurospora.{{Citation |title=Reproductive isolation and phylogenetic divergence in Neurospora: Comparing methods of species recognition in a model eukaryote | author=Jeremy R. Dettman, David J. Jacobson, Elizabeth Turner, Anne Pringle, and John W. Taylor | journal=Evolution | year=2003 | volume=57 | issue=12 | pages=2721–2741 | doi=10.1554/03-074 | pmid=14761052| s2cid=198153854 }} In crosses between different species in the genera, sympatric pairs show low reproductive success, significantly lower than allopatric pairs. This pattern is observed across small and large geographic scales, with distance correlating with reproductive success. Further evidence of reinforcement in the species was the low fitness detected in the hybrids create from crosses, and that no hybrids have been found in nature, despite close proximity.

Ethological isolation has been observed between some mosquito species in the Southeast Asian Aedes albopictus group, suggesting—from laboratory experiments of mating trials—that selection against hybrids is occurring, in the presence of reproductive character displacement.{{Citation |title=Reinforcement for ethological isolation in the southeast asian Aedes albopictus subgroup (Diptera: Culicidae) | author=Denson Kelly McLain and Karamjit S. Rai | journal=Evolution | year=1986 | volume=40 | issue=60 | pages=1346–1350 | doi=10.1111/j.1558-5646.1986.tb05759.x | pmid=28563509| s2cid=26849954 | doi-access=free }}

Female mate discrimination is increased with intermediate migration rates between allopatric populations of Timema cristinae (genus Timema) compared to high rates of migration (where gene flow impedes selection) or low rates (where selection is not strong enough).{{Citation |title=Reproductive isolation driven by the combined effects of ecological adaptation and reinforcement | author=Patrik Nosil, Bernard J. Crespi, and Cristina P. Sandoval | journal=Proceedings of the Royal Society B | year=2003 | volume=270 | issue=1527 | pages=1911–1918 | doi=10.1098/rspb.2003.2457 | pmid=14561304| pmc=1691465 }}{{Citation |title=Natural selection and divergence in mate preference during speciation | author=Patrik Nosil, Bernard J. Crespi, Regine Gries, and Gerhard Gries | journal=Genetica | year=2007 | volume=129 | issue= 3| pages=309–327 | doi=10.1007/s10709-006-0013-6 | pmid=16900317 | s2cid=10808041 }}

File:Distribution magicicada usa fixed.png in the U.S. The yellow area corresponds to the sympatric overlap of Magicicada neotredecim (blue) with Magicicada tredecim (red).]]

Where the ranges of the cicada species Magicicada tredecim and M. neotredecim overlap (where they are sympatric), the pitch of M. neotredecim male calling songs is roughly 1.7 kHz compared to 1.1 kHz for those of M. tredecim, with corresponding female song pitch preference differences.{{Citation |title=Allochronic speciation, secondary contact, and reproductive character displacement in periodical cicadas (Hemiptera: Magicicada spp.): genetic, morphological, and behavioural evidence | author=John R. Cooley, Chris Simon, David C. Marshall, Karen Slon, and Christopher Ehrhardt | journal=Molecular Ecology | year=2001 | volume=10 | issue=3 | pages=661–671 | doi=10.1046/j.1365-294x.2001.01210.x | pmid=11298977| bibcode=2001MolEc..10..661C | s2cid=24760583 }} In allopatric M. neotredecim populations, the mating call pitch is 1.3–1.5 kHz. The biogeography of the cicadas suggests that M. neotredecim originated after the retreat of the last glacial advance in North America.

The song differences of Laupala crickets on the Hawaiian Islands appear to exhibit patterns consistent with character displacement in sympatric populations.Roger K. Butlin (1989). Reinforcement of premating isolation. In Otte, D. and Endler, John A. (eds) Speciation and its Consequences, Sinauer Associates, pp. 158–179, {{ISBN|0-87893-657-2}} A similar pattern exists with Allonemobius fasciatus and A. socius, species of ground crickets in eastern North America.{{Citation |title=Calling song displacement in a zone of overlap and hybridization | author=J. H. Benedix Jr. and Daniel J. Howard | journal=Evolution | year=1991 | volume=45 | issue=8 | pages=1751–1759 | doi=10.1111/j.1558-5646.1991.tb02685.x | pmid=28563959| s2cid=46400422 | doi-access=free }}

Males in sympatric populations of the damselflies Calopteryx maculata and C. aequabilis are able to discriminate between females of different species better than those in allopatric populations; with females of C. aequabilis in sympatric populations exhibiting lighter wing colors compared to allopatric females—an illustration of reproductive character displacement.{{Citation |title=Reproductive Isolation and the Potential for Character Displacement in the Damselflies, Calopteryx Maculata and C. Aequabilis (Odonata: Calopterygidae) | author=Jonathan K. Waage | journal=Systematic Biology | year=1975 | volume=24 | issue=1 | pages=24–36 | doi=10.1093/sysbio/24.1.24 }}{{Citation |title=Reproductive character displacement in Calopteryx (Odonata: Calopterygidae | author=Jonathan K. Waage | journal=Evolution | year=1979 | volume=33 | issue=1 | pages=104–116 | doi=10.1111/j.1558-5646.1979.tb04667.x | pmid=28568062| s2cid=43039210 }}

Fifteen species of sympatrically distributed Agrodiaetus butterflies with pronounced differences in wing color pattern likely arose as a result of speciation by reinforcement.{{Citation |title=Reinforced butterfly speciation | author=C. D. Jiggins | journal=Heredity | year=2006 | volume=96 | issue= 2| pages=107–108 | doi=10.1038/sj.hdy.6800754 | pmid=16222327 | s2cid=24389006 | doi-access=free }} Phylogenetic patterns indicate the differences arose in allopatry and were reinforced when the distributions came into secondary contact.{{Citation |title=Reinforcement of prezygotic isolation and karyotype evolution in Agrodiaetus butterflies | author=Vladimir A. Lukhtanov, Nikolai P. Kandul, Joshua B Plotkin, Alexander V. Dantchenko, David Haig, and Naomi E. Pierce | journal=Nature | year=2005 | volume=436 | issue=7049 | pages=385–389 | doi=10.1038/nature03704 | pmid=16034417| bibcode=2005Natur.436..385L | s2cid=4431492 }}

File:Drosophila melanogaster - side (aka).jpg fruit fly]]

Drosophila is one of the most studied species in speciation research.{{Citation |title=What does Drosophila genetics tell us about speciation? | author=James Mallet | journal=Trends in Ecology & Evolution | year=2006 | volume=21 | issue=7 | pages=386–393 | doi=10.1016/j.tree.2006.05.004 | pmid=16765478}} Dobzhansky and Koller were the first to study isolation between Drosophila species.{{rp|358}} Since then, other studies of natural populations such as the D. paulistorum races exhibiting stronger isolation in sympatry versus allopatry,{{Citation |title=Direct Observation of Sexual Isolation between Allopatric and between Sympatric Strains of the Different Drosophila paulistorum Races | author=Lee Ehrman | journal=Evolution | year=1965 | volume=19 | issue=4 | pages=459–464 | doi=10.2307/2406243 | jstor=2406243 | author-link=Lee Ehrman }} or the enhanced isolation found in sympatric populations of D. mojavensis and D. arizonae in southwest America.{{Citation |title=Character displacement for sexual isolation between Drosophila mojavensis and Drosophila arizonensis | author=Marvin Wasserman and H. Roberta Koepfer | journal=Evolution | year=1977 | volume=31 | issue=4 | pages=812–823 | doi=10.1111/j.1558-5646.1977.tb01073.x | pmid=28563708| s2cid=36693544 }} Rare, sterile hybrids form between D. pseudoobscura and D. persimilis, with sympatric D. pseudoobscura females discriminating against D. persimilis males; more so than allopatric populations.{{Citation |title=Speciation driven by natural-selection in Drosophila | author=Mohamed A. F. Noor | journal=Nature | year=1995 | volume=375 | issue=6533 | pages=674–675 | doi=10.1038/375674a0 | pmid=7791899 | bibcode=1995Natur.375..674N | s2cid=4252448 }} Other Drosophila research on reinforcement has been from laboratory experiments and is discussed below. On the east coast of Australia, D. serrata shares a zone of sympatric overlap with the closely related species D. birchii.{{Citation |title=Are Traits That Experience Reinforcement Also Under Sexual Selection? | author=Megan Higgie and Mark W. Blows | journal=The American Naturalist | year=2007 | volume=170 | issue=3 | pages=409–420 | doi=10.1086/519401 | pmid=17879191| bibcode=2007ANat..170..409H | s2cid=44985193 | url=http://espace.library.uq.edu.au/view/UQ:129790/UQ129790_OA.pdf }} The species exhibits reproductive character displacement, with sexual selection operating on the hydrocarbons of the flies cuticle.{{Citation |title=Natural Selection and the Reinforcement of Mate Recognition | author=Megan Higgie, Steve Chenoweth, and Mark W. Blows | journal=Science | year=2000 | volume=290 | issue=5491 | pages=519–521 | doi=10.1126/science.290.5491.519 | pmid=11039933 | bibcode=2000Sci...290..519H | url=https://espace.library.uq.edu.au/view/UQ:10714/Higgie_et_al_200.pdf }} Reinforcement appears to be driving their speciation in nature, supported by simulated experimental laboratory populations.{{Citation |title=The Evolution of Reproductive Character Displacement Conflicts with how Sexual Selection Operates within a Species | author=Megan Higgie and Mark W. Blows | journal=Evolution | year=2008 | volume=62 | issue=5 | pages=1192–1203 | doi=10.1111/j.1558-5646.2008.00357.x | pmid=18298640| s2cid=333466 | doi-access=free }}{{Citation |title=Speciation via species interactions: the divergence of mating traits within species | author=Conrad J. Hoskin and Megan Higgie | journal=Ecology Letters | year=2010 | volume=13 | issue=4 | pages=409–420 | doi=10.1111/j.1461-0248.2010.01448.x | pmid=20455922 | bibcode=2010EcolL..13..409H }}

The deer mice Peromyscus leucopus and P. gossypinus exhibit reproductive character displacement in mating preferences, with heterospecific matings taking place between the species.{{Citation |title=Ethological isolation in the cenospecies Peromyscus leucopus | author=H. MacCarley | journal=Evolution | year=1964 | volume=18 | issue= 2| pages=331–342 | doi= 10.1111/j.1558-5646.1964.tb01605.x| s2cid=84959325 | doi-access=free }}

File:Neptunea - links&rechts gewonden.jpgs, like those of Partula can coil in sinistral and dextral directions such as these, Neptunea angulata (left) and N. despecta (right) shells.]]

Partula suturalis is polymorphic for shell chirality in that it has two forms: sinistral (left-handed) and dextral (right-handed) shells, unlike other monomorphic species on the island of Mo'orea which have only one form (with the exception of P. otaheitana).{{Citation |title=Polymorphism for direction of coil in Partula suturalis: Behavioral isolation and positive frequency dependent selection | author=Michael S. Johnson | journal=Heredity | year=1982 | volume=49 | issue=2 | pages=145–151 | doi= 10.1038/hdy.1982.80| doi-access=free }} This polymorphic trait has a direct effect on mate choice and mating behavior; as shown in laboratory mating tests that opposite-coil pairs mate much less often. In areas where P. suturalis lives sympatrically with other sinistral and dextral Partula species, the opposite P. suturalis morph is typically present.{{Citation |title=Speciation by Reinforcement | author=Roger Butlin | journal=Trends in Ecology & Evolution | year=1987 | volume=2 | issue=1 | pages=8–13 | doi= 10.1016/0169-5347(87)90193-5| pmid=21227808 | bibcode=1987TEcoE...2....8B }} Butlin succinctly describes one example of this unique pattern:

P. suturalis is sympatric with the dextral P. aurantia and sinistral P. olympia, whose ranges abut but do not overlap; P. suturalis is sinestral in the range of P. aurantia and dextral in the range of P. olympia and does not normally hybridize with either species. However, where their ranges meet there is a sharp transition in the coil of P. suturalis and in this transition zone it hybridizes with both P. aurantia and P. olympia.

The reversal in chirality to sinistrality must have evolved as an isolating mechanism,{{Citation |title=The genus Partula on Moorea: speciation in progress | author=J. Murray and B. Clarke | journal=Proceedings of the Royal Society B | year=1980 | volume=211 | issue= 1182| pages=83–117 | doi= 10.1098/rspb.1980.0159| bibcode=1980RSPSB.211...83M | s2cid=85343279 }} with patterns of reproductive character displacement suggesting speciation by reinforcement.

Satsuma largillierti lives on the western half of Okinawa Island while Satsuma eucosmia lives on the eastern half. Both populations overlap in sympatry along the middle of the island, where the penis length of the species differs significantly in sympatry (a case of reproductive character displacement{{Citation|title=Evolution|date=2016|author=Carl T. Bergstrom and Lee Alan Dugatkin|pages=508–509|edition=2nd|publisher=W. W. Norton & Company|isbn=9780393937930}}), but not in allopatry.{{Citation|title=Reproductive Character Displacement in Genital Morphology in Satsuma Land Snails|year=2009|author=Yuichi Kameda, Atsushi Kawakita, and Makoto Kato|journal=The American Naturalist|volume=173|issue=5|pages=689–697|doi=10.1086/597607 | pmid=19298185|bibcode=2009ANat..173..689K |s2cid=13428948 }} A similar pattern in snails is found with Lymnaea peregra and L. ovata in the Swiss lake Seealpsee; with mating signal acting as the sympatrically displaced trait.{{Citation |title=Reproductive character displacement between the closely related freshwater snails Lymnaea peregra and L. ovata | author=Esther B. Wullschleger, Jürgen Wiehn, and Jukka Jokela | journal=Evolutionary Ecology Research | year=2002 | volume=4 | pages=247–257 }}

The abalone genus Haliotis has 19 species that occur in sympatry and one that occurs in allopatry. Of the sympatric species, they all contain sperm lysin that drives gamete isolation, but the allopatric species does not.{{Citation |title=Positive selection is a general phenomenon in the evolution of abalone sperm lysin | author=Y. H. Lee, T. Ota, and V. D. Vacquier | journal=Molecular Biology and Evolution | year=1995 | volume=12 | issue=2 | pages=231–238 | doi= 10.1093/oxfordjournals.molbev.a040200| pmid=7700151| doi-access=free }}{{rp|343}} A similar pattern of sperm lysin differentiation is found in the mussel species Mytilus galloprovincialis and M. trossulus and has likely occurred within the last 200 years due to human-mediated distribution by ships.{{rp|343}}

Plants are thought to provide suitable conditions for reinforcement to occur. This is due to a number of factors such as the unpredictability of pollination, pollen vectors, hybridization, hybrid zones, among others. The study of plants experiencing speciation by reinforcement has largely been overlooked by researchers;{{rp|364}} however, there is evidence of its occurrence in them.{{Citation |title=Reinforcement in plants | author=Robin Hopkins | journal=New Phytologist | year=2013 | volume=197 | issue=4 | pages=1095–1103 | doi=10.1111/nph.12119 | pmid=23495388 | doi-access=free | bibcode=2013NewPh.197.1095H }}

In the Texas wildflower Phlox drummondii, cis-regulatory mutations of genes that code for anthocyanin pigmentation have caused genetic divergence of two populations.{{Citation |title=Identification of two genes causing reinforcement in the Texas wildflower Phlox drummondii | author=Robin Hopkins and Mark D. Rausher| journal=Nature | year=2011 | volume=469 | issue=7330| pages=411–414 | doi=10.1038/nature09641 | pmid=21217687| bibcode=2011Natur.469..411H| s2cid=205223257}} Hybrids (between P. drummondii and P. cuspidata) with maladaptive, intermediate characteristics are under-pollinated; increasing reproductive isolation through reinforcement. The maintenance of the ancestral flower color in the allopatric population is favored weakly by selection, where the derived color in the sympatric population is being driven by strong selection.{{Citation |title=Strong Reinforcing Selection in a Texas Wildflower | author=Rob Hopkins, Rafael F. Guerrero, Mark D. Rausher, and Mark Kirkpartrick | journal=Current Biology | year=2014 | volume=24 | issue=17 | pages=1995–1999 | doi=10.1016/j.cub.2014.07.027 | pmid=25155503| doi-access=free | bibcode=2014CBio...24.1995H }} Similarly, in P. pilosa and P. glaberrima, character displacement of petal color has been driven by selection, aided by pollen discrimination.{{Citation |title=Natural selection for reproductive isolation in Phlox | author=Donald A. Levin and Harold W. Kerster | journal=Evolution | year=1967 | volume=21 | issue=4 | pages=679–687 | doi= 10.1111/j.1558-5646.1967.tb03425.x | pmid=28563087| s2cid=13457880 | doi-access=free }} Displacement in flower size has also been observed in the nightshade species Solanum grayi and S. lymholtzianum in sympatry as well as S. rostratum and S. citrullifolium.{{Citation |title=Reproductive Character Displacement and Floral Diversity in Solanum Section Androceras | author=Michael D. Whalen | journal=Systematic Biology | year=1978 | volume=3 | issue=1 | pages=77–86 | doi= 10.2307/2418533| jstor=2418533 }}

{{multiple image | align = right | image1 = Pinus muricata-1.jpg | width1 = 800 | caption1 = Green southern population foliage of Pinus muricata | image2 = Pinus muricata foliage Mendocino.jpg | width2 = 800 | caption2 = Blue northern population| total_width = 350 | height1 = 500 | height2 = 500 }}

The bishop pine is divided into two populations distinguished by monoterpene, stomata, and alloenzyme differences; flowering time; and needle color: blue foliage in the northern population and green foliage in the southern populations in California.{{Citation |title=A steep cline in Pinus muricata | author=Constance I. Millar |author-link1=Constance I. Millar | journal=Evolution | year=1983 | volume=37 | issue=2 | pages=311–319 | doi=10.1111/j.1558-5646.1983.tb05541.x | pmid=28568365| s2cid=34080334 | doi-access=free }} A small region exists where the species meet in a cline—sustained by selection due to a flowering time divergence, thought to represent reinforcement taking place.

Similar patterns of both character displacement in sympatric populations of species have been documented in:{{rp|361}}

• Agrostis tenuis{{Citation |title=Evolution in closely adjacent plant populations. IV. Barriers to gene flow | author=Thomas McNeilly and Janis Antonovics | journal=Heredity | year=1968 | volume=23 | issue= 2| pages=205–218 | doi=10.1038/hdy.1968.29 | doi-access=free }}
• Anthoxanthum odoratum
• Gilia{{Citation |title=The selective origin of incompatibility barriers in the plant genus Gilia | author=Verne Grant | journal=The American Naturalist | year=1966 | volume=100 | issue=911 | pages=99–118 | doi=10.1086/282404 | bibcode=1966ANat..100...99G | s2cid=84918503 }}
• Costus plants: Costus allenii, C. laevis, and C. guanaiensis;{{Citation |title=Floral convergence and pollinator sharing in two bee-pollinated tropical herbs | author=Douglas W. Schemske | journal=Ecology | year=1981 | volume=62 | issue=4 | pages=946–954 | doi=10.2307/1936993 | jstor=1936993 | bibcode=1981Ecol...62..946S }}{{Citation |title=Pollinator assemblages and visitation rates for 11 species of neotropical Costus (Costaceae) | author=Kathleen M. Kay and Douglas W. Schemske | journal=Biotropica | year=2003 | volume=35 | issue=2 | pages=198–207 | doi=10.1646/02159 | s2cid=198158311 }} C. pulverulentus and C. scaber{{Citation |title=Natural selection reinforces speciation in a radiation of neotropical rainforest plants| author=Kathleen M. Kay and Douglas W. Schemske | journal=Evolution | year=2008 | volume=62 | issue=10 | pages=2628–2642 | doi=10.1111/j.1558-5646.2008.00463.x | pmid=18637960| s2cid=205781802 | doi-access=free }}
• A unique case of post-zygotic instead of prezygotic isolation has been observed in both Gossypium and Gilia, suggesting that in plants, post-zygotic isolation's role in reinforcement may play a larger role.{{rp|361}}
• Sympatric populations of Juncus effusus (common rush) exhibits genetic differentiation of plants that flower at different times preventing hybridization.{{Citation|title=Separation in flowering time contributes to the maintenance of sympatric cryptic plant lineages |author=Stefan G Michalski and Walter Durka |journal=Ecology and Evolution |year=2015 |volume=5 |issue=11 |pages=2172–2184 |doi=10.1002/ece3.1481 |pmid=26078854 |pmc=4461419 |bibcode=2015EcoEv...5.2172M |url= }} Allochrony may play a role.{{Citation|title=The role of allochrony in speciation |author=Rebecca S. Taylor and Vicki L. Friesen |journal=Molecular Ecology |year=2017 |volume=26 |issue=13 |pages=3330–3342 |doi=10.1111/mec.14126 |pmid= 28370658 |s2cid=46852358 |doi-access=free |bibcode=2017MolEc..26.3330T }}

File:Enhanced pre-zygotic isolation in Drosophila (allopatric & sympatric plots-vert).png. Gradients indicate the predictions of reinforcement for allopatric and sympatric populations.{{Citation |title="Patterns of Speciation in Drosophila" Revisited | author=Jerry A. Coyne and H. Allen Orr | journal=Evolution | year=1997 | volume=51 | issue=1 | pages=295–303 | doi=10.1111/j.1558-5646.1997.tb02412.x | pmid=28568795| s2cid=40390753 | doi-access=free }}]]Assortive mating is expected to increase among sympatric populations experiencing reinforcement. This fact allows for the direct comparison of the strength of prezygotic isolation in sympatry and allopatry between different experiments and studies.{{rp|362}} Jerry Coyne and H. Allen Orr surveyed 171 species pairs, collecting data on their geographic mode, genetic distance, and strength of both prezygotic and post-zygotic isolation; finding that prezygotic isolation was significantly stronger in sympatric pairs, correlating with the ages of the species.{{rp|362}} Additionally, the strength of post-zygotic isolation was not different between sympatric and allopatric pairs.

This finding lends support the predictions of speciation by reinforcement and correlates well with another later study by Daniel J. Howard.{{rp|363}} In his study, 48 studies with observed reproductive character displacement (including plants, insects, crustaceans, molluscs, fish, amphibians, reptiles, birds, and mammals) were analyzed. The cases met several criteria such as the trait in question serving as a reproductive barrier and if there existed clear patterns of sympatry versus allopatry. Out of the 48 candidates, 69 percent (33 cases) found enhanced isolation in sympatry, suggesting that the pattern predicted by reinforcement is common in nature. In addition to Howard's comparative study, he guarded against the potential for positive-result publication bias by surveying 37 studies of hybrid zones. A prediction of reinforcement is that assortive mating should be common in hybrid zones; a prediction that was confirmed in 19 of the 37 cases.

A survey of the rates of speciation in fish and their associated hybrid zones found similar patterns in sympatry, supporting the occurrence of reinforcement.A. R. McCune and N. R. Lovejoy. (1998). The relative rate of sympatric and allopatric speciation in fishes. In D. J. Howard and S. H. Berlocher (eds) Endless Forms: Species and Speciation, Oxford University Press, pp. 172–185. One study in the plants Glycine and Silene; however, did not find enhanced isolation.{{Citation |title=Patterns of reproductive isolation in three angiosperm genera |author=Leonie C. Moyle, Matthew S Olson, and Peter Tiffin |journal=Evolution |year=2004 |volume=58 |issue=6 |pages=1195–1208 |doi=10.1554/03-511 |pmid=15266970 |s2cid=198156807 }}

{{see also|Laboratory experiments of speciation}}

Laboratory studies that explicitly test for reinforcement are limited.{{rp|357}} In general, two types of experiments have been conducted: using artificial selection to mimic natural selection that eliminates the hybrids (often called "destroy-the-hybrids"), and using disruptive selection to select for a trait (regardless of its function in sexual reproduction).{{rp|355–357}} Many experiments using the destroy-the-hybrids technique are generally cited as supportive of reinforcement; however, some researchers such as Coyne and Orr and William R. Rice and Ellen E. Hostert contend that they do not truly model reinforcement, as gene flow is completely restricted between two populations.{{Citation|title=Laboratory Experiments on Speciation: What Have We Learned in 40 Years?| year=1993 | author=William R. Rice and Ellen E. Hostert | journal=Evolution | volume=47 | issue=6 | pages=1637–1653 | doi=10.1111/j.1558-5646.1993.tb01257.x | pmid=28568007| s2cid=42100751 }}{{rp|356}} The table below summarizes some of the laboratory experiments that are often cited as testing reinforcement in some form.

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Category:Evolutionary biology

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