Ecological speciation

Divergent selection is key to the occurrence of ecological speciation. Three ecological causes of divergent selection have been identified: differences in environmental conditions, ecological interactions, and sexual selection. The causes are outlined in the following list:{{Citation|title=Speciation by Natural and Sexual Selection: Models and Experiments |author=Kirkpatrick, Mark & Ravigné, Virginie |journal=The American Naturalist |year=2002 |volume=159 |pages=S22–S35 |doi=10.1086/338370 |pmid=18707367|s2cid=16516804 }}{{Citation|title=Ecology and the origin of species |author=Dolph Schluter |journal=Trends in Ecology & Evolution |year=2001 |volume=16 |issue=17 |pages=327–380 |doi=10.1016/S0169-5347(01)02198-X |pmid=11403870 |s2cid=9845298 }}

[[File:Hypothetical experimental tests for ecological speciation from environmental differences.svg|right|thumb|upright=1.2|Two types of experimental tests of ecological speciation caused by divergent environments.

Experiment 1: a speciation event predicted to have occurred due to an ecologically-based divergent factor giving rise to two new species (1a). The experiment produces viable and fertile hybrid offspring and places them in isolated settings that match their parental environments (1b). The experiment predicts that, "reproductive isolation should then evolve in correlation with environment, building [increasing] between populations in different environments and being absent between laboratory and natural populations from similar environments."

Experiment 2: a peripatric speciation event between a mainland species and an isolated endemic population occurs (2a). A laboratory setting replicates the mainland environmental conditions thought to have driven speciation and a mainland population is placed within it. The experiment predicts that the transplant will show evidence of isolation that matches that of the island endemic (2b).]]

• Differences in environmental conditions as a prerequisite to speciation is incontrovertibly the most studied. Predation, resource availability (food abundance), climatic conditions, and the structure of a habitat are some of the examples that can differ and give rise to divergent selection.{{Citation|title=The Ecology of Adaptive Radiation |author=Dolph Schluter |date=2000 |publisher=Oxford University Press |isbn=0198505221 }} Despite being one of the most studied factors in ecological speciation, many aspects are still less understood such as how prevalent the process is in nature as well as the origin of barriers for post-zygotic isolation (as opposed to the much easier detectable pre-zygotic barriers).{{rp|181}} Laboratory experiments involving single-environmental differences are limited and have often not tracked the traits involved in isolation. Studies in nature have focused on a variety of environmental factors such as predation-caused divergent selection; however, little has been studied in regards to pathogens or parasites.
• Ecological interactions can drive divergent selection between populations in sympatry. Examples of these interactions can be intraspecific (between the same species) and interspecific (between different species) competition{{Citation|title=Character Shifts of Prey Species That Share Predators |author=Peter A. Abrams |journal=American Naturalist |year=2000 |volume=154 |issue=4 |pages=45–61 |doi=10.1086/303415 |pmid=29592581 |s2cid=4387648 }} or relationships such as those of ecological facilitation.{{Citation|title=Competitive and Facilitative Evolutionary Diversification |author=Troy Day and Kyle A. Young |journal=BioScience |year=2004 |volume=54 |issue=2 |pages=101–109 |doi=10.1641/0006-3568(2004)054[0101:CAFED]2.0.CO;2 |doi-access= |s2cid=41757319 }}{{Citation|title=Evolutionary Branching and Sympatric Speciation Caused by Different Types of Ecological Interactions |author=Michael Doebeli and Ulf Dieckmann |journal=American Naturalist |year=2000 |volume=156 |issue=4 |pages=77–101 |doi=10.1086/303417 |pmid=29592583|s2cid=4409112 }} Interspecific competition in particular has support from experiments; however it is unknown if it can give rise to reproductive isolation despite driving divergent selection. Reinforcement (the strengthening of isolation by selection favoring the mating of members of their own populations due to reduced fitness of hybrids) is considered to be a form of, or involved in, ecological speciation.{{Citation |title=The Role of Reinforcement in Speciation: Theory and Data |author1=Maria R. Servedio |author2=Mohamed A. F. Noor |author2-link=Mohamed Noor |journal=Annual Review of Ecology, Evolution, and Systematics |year=2003 |volume=34 |pages=339–364 |doi=10.1146/annurev.ecolsys.34.011802.132412 }} Though, debate exists as to how to determine ultimate causes since reinforcement can complete the speciation process regardless of how it originated.{{Citation |title=Reinforcement during ecological speciation | author=Mark Kirkpatrick | journal=Proceedings of the Royal Society B | year=2001 | volume=268 | issue=1473 | pages= 1259–1263| doi=10.1098/rspb.2000.1427 | pmid=11410152 | pmc=1088735 }} Further, character displacement can have the same effect.
• Sexual selection can play a role in ecological speciation as the recognition of mates is central to reproductive isolation{{Citation|title=Sexual selection and speciation |author=Tami M. Panhuisa, Roger Butlin, Marlene Zuk, and Tom Tregenza |journal=Trends in Ecology & Evolution |year=2001 |volume=16 |issue=7 |pages=364–371 |doi=10.1016/S0169-5347(01)02160-7 |pmid=11403869 }}—that is, if a species cannot recognize its potential mates, the flow of genes is suspended. Despite its role, only two types of sexual selection can be implicated in ecological speciation: the spatial variation in secondary sexual traits (sexual traits that arise specifically at sexual maturity){{Citation|title=Rapid origin of sexual isolation and character divergence in a cline |author=Russell Lande |journal=Evolution |year=1982 |volume=36 |issue=2 |pages=213–223 |doi=10.1111/j.1558-5646.1982.tb05034.x |pmid=28563171 |s2cid=20428163 |doi-access= }} or communication and mating systems.{{Citation|title=How sensory drive can promote speciation |author=Janette Wenrick Boughman |journal=Trends in Ecology & Evolution |year=2002 |volume=17 |issue=12 |pages=571–577 |doi=10.1016/S0169-5347(02)02595-8 }} This restriction is based on the fact that they produce diverging environments in which selection can act. For example, isolation will increase between two populations where there is a mismatch between signals (such as the feather display of a male bird) and the preferences (such as the sexual preferences of a female bird). This pattern has been detected in stickleback fish.{{Citation|title=Divergent sexual selection enhances reproductive isolation in sticklebacks |author=Janette Wenrick Boughman |journal=Nature |year=2001 |volume=411 |issue=6840 |pages=944–948 |doi=10.1038/35082064 |pmid=11418857 |bibcode=2001Natur.411..944B |s2cid=5669795 }}

File:Ecological Speciation (habitat isolation) Schematic.svg interspersed with grassland) or a gradient (such as forest transitioning gradually into shrub or grassland.]]

Populations of a species can become spatially isolated due to preferences for separate habitats. The separation decreases the chance of mating to occur between the two populations, inhibiting gene flow, and promoting pre-zygotic isolation to lead to complete speciation. Habitat isolation is not equivalent to a geographic barrier like that of allopatric speciation.{{rp|182}} Instead, it is based on genetic differences, where one species is unable to exploit a different environment, resulting from fitness advantages, fitness disadvantages, or resource competition.{{rp|182}}

Jerry Coyne and H. Allen Orr posit two different forms of habitat isolation: microspatial habitat isolation (where matings between two species are reduced by preferences or adaptations to ecologically differing areas, despite occupying the same generalized area) and macrospatial habitat isolation (defined by fully allopatric habitats that inhibit gene flow.){{rp|182–3}} Identification of both forms of habitat isolation in nature is difficult due to the effects of geography. Measuring microspatial isolation demands several factors:{{rp|184}}

• the spatial separation of different species' members is greater than those of members of the same species
• during simultaneous breeding periods, the spatial separation reduces gene flow
• decreased gene flow is directly the result of decreased mating
• genetic differences correspond to the spatial separation

Allopatric distributions pose several problems for detecting true habitat isolation in that different habitats of two allopatrically isolated species does not imply ecologically caused speciation. Alternative explanations could account for the patterns:{{rp|185}}

• species differences may be caused by geographic isolation
• the species may or may not occupy different habitats if they existed in sympatry
• in cases of similar habitats in allopatry, species may be adapted to unknown ecological factors
• if the species existed in sympatry, competition may drive habitat segregation that would be undetectable in allopatry

These issues (with both micro- and macro-spatial isolation) can be overcome by field or laboratory experiments such as transplantation of individuals into opposite habitats{{rp|185}} (though this can prove difficult if individuals are not completely unfit for the imposed habitat).{{rp|186}} Habitat isolation can be measured for a species pair ($a$ and $b$) during a breeding period by:

$1-\backslash frac\{p\_\{ab\}\}\{2p\_ap\_b\}$

Here, $p\_\{ab\}$ is the proportion of encounters between matings that involve partners of a different species that are observed. $p\_a$ is the proportion of total individuals of species $a$. $p\_b$ is the proportion of total individuals of species $b$. The expected proportion of mating encounters between different species if mating is random is denoted by $2\; p\_a\; p\_b$. A statistic of $1$ indicates no mating encounters of different species where $0$ indicates random mating of different species.

Ecological speciation caused by habitat isolation can occur in any geographic sense, that is, either allopatrically, parapatrically, or sympatrically. Speciation arising by habitat isolation in allopatry (and parapatry) is straightforward in that reduced gene flow between two populations acquire adaptations that fit the ecological conditions of their habitat. The adaptations are reinforced by selection and, in many cases such as with animals, are reinforced by behavioral preferences (e.g. in birds that prefer specific vocalizations).{{rp|189}} A classic example of habitat isolation occurring in allopatry is that of host-specific cospeciation{{rp|189}} such as in the pocket gophers and their host chewing lice{{cite journal |author=Roderic DM Page |title=Cospeciation |journal=eLS |publisher=John Wiley & Sons Ltd |location=Chichester |date=2005 |doi=10.1038/npg.els.0004124|isbn=0470016175 }} or in the fig wasp-fig tree relationship and the yucca-yucca moth relationship—examples of ecological speciation caused by pollinator isolation.{{rp|189}} In sympatry, the scenario is more complex, as gene flow may not be reduced enough to permit speciation. It is thought that selection for niche divergence can drive the process. In addition, if sympatry results from the secondary contact of two previously separated populations, the process of reinforcement, the selection against unfit hybrids between the two populations, may drive their complete speciation. Competition for resources may also play a role.{{rp|191}}

File:Sagebrushsjc.jpg]]

Habitat isolation is a significant impediment to gene flow and is exhibited by the common observation that plants and animals are often spatially separated in relation to their adaptations.{{rp|183}} Numerous field studies, transplantation and removal experiments, and laboratory studies have been conducted to understand the nature of speciation caused by habitat isolation.{{rp|186–188}} Horkelia fusca, for example, grows on California slopes and meadows above 4500 feet, where its closet relatives H. californica and H. cuneata grow below 3200 feet in coastal habitats. When species are transplanted to alternate habitats, their viability is reduced, indicating that gene flow between the populations is unlikely.{{Citation|title=Narrow Hybrid Zone Between Two Subspecies of Big Sagebrush (Artemisia Tridentata: Asteraceae). IV. Reciprocal Transplant Experiments |author=Han Wang, E. Durant McArthur, Stewart C. Sanderson, John H. Graham, & D. Carl Freeman |journal=Evolution |year=1997 |volume=51 |issue=1 |pages=95–102 |doi=10.1111/j.1558-5646.1997.tb02391.x |pmid=28568779 |s2cid=19274910 |doi-access=free }} Similar patterns have been found with Artemisia tridentata tridentata and A. tridentata subsp. vaseyana in Utah, where hybrid zones exists between altitudinal populations, and transplant experiments reduce the fitness of the subspecies.{{Citation|title=Experimental Studies on the Nature of Species. I. Effect of Varied Environments on Western North American Plants |author=Jens Clausen, David D. Keck, & William M. Hiesey |date=1940 |publisher=Carnegie Institution of Washington |location=Washington D.C. |isbn=9780608062204 }}

Speciation by habitat isolation has also been studied in serpentine leaf miner flies,{{Citation|title=Sympatric genetic divergence in the leaf-mining insect Liriomyza brassicae (Dipter: Agromyzidae) |author=Salvatore J. Tavormina |journal=Evolution |year=1982 |volume=36 |issue=3 |pages=523–534 |doi=10.1111/j.1558-5646.1982.tb05073.x |pmid=28568038 |s2cid=29041437 }} ladybird beetles (Epilachna),{{Citation|title=Reproductive Isolation by Host Specificity in a Pair of Phytophagous Ladybird Beetles |author=Haruo Katakura, Miyuki Shioi, & Yumi Kira |journal=Evolution |year=1989 |volume=43 |issue=5 |pages=1045–1053 |doi=10.1111/j.1558-5646.1989.tb02549.x |pmid=28564150 |s2cid=22996209 |doi-access=free }} goldenrod gall flies,{{Citation|title=Behavioral Evidence for Host-race Formation in Eurosta Solidaginis |author=Timothy P. Craig, Joanne K. Itami, Warren G. Abrahamson, John D. Horner |journal=Evolution |year=1993 |volume=47 |issue=6 |pages=1696–1710 |doi=10.1111/j.1558-5646.1993.tb01262.x |pmid=28567992 |s2cid=205778515 |doi-access=free }} Rhagoletis pomonella,{{Citation|title=Host fidelity is an effective premating barrier between sympatric races of the apple maggot fly |author=Jeffrey L. Feder, Susan B. Opp, Brian Wlazlo, Katherine Reynolds, Wesley Go, & Steve Spisak |journal=PNAS |year=1994 |volume=91 |issue=17 |pages=7990–7994 |doi=10.1073/pnas.91.17.7990 |pmid=11607491 |pmc=44530 |bibcode=1994PNAS...91.7990F |doi-access=free }}{{Citation|title=Fruit odor discrimination and sympatric host race formation in Rhagoletis |author=Charles Linn Jr., Jeffrey L. Feder, Satoshi Nojima, Hattie R. Dambroski, Stewart H. Berlocher, & Wendell Roelofs |journal=PNAS |year=2003 |volume=100 |issue=20 |pages=11490–11493 |doi=10.1073/pnas.1635049100 |pmid=14504399 |pmc=208785 |bibcode=2003PNAS..10011490L |doi-access=free }} leaf beetles,{{Citation|title=Isolating a role for natural selection in speciation: Host adaptation and sexual isolation in Neochlamisus bebbianae leaf beetles |author=Daniel J. Funk |journal=Evolution |year=1998 |volume=52 |issue=6 |pages=1744–1759 |doi=10.1111/j.1558-5646.1998.tb02254.x |pmid=28565322 |s2cid=22704901 |doi-access=free }} and pea aphids.{{Citation|title=Reproductive isolation between sympatric races of pea aphids. I. Gene flow restriction and habitat choice |author=Sara Via |journal=Evolution |year=1999 |volume=53 |issue=5 |pages=1446–1457 |doi=10.1111/j.1558-5646.1999.tb05409.x |pmid=28565574 |s2cid=28392433 |doi-access=free }}

Ecological speciation due to sexual isolation results from differing environmental conditions that modify communication systems or mate choice patterns over time. Examples abound in nature. The coastal snail species Littorina saxatilis has been a focus of research as two ecotypes residing at different shore levels exhibit reproductive isolation as a result of mate choice regarding the body size differences of the ecotype.{{Citation|title=Testing alternative models for sexual isolation in natural populations of Littorina saxatilis: indirect support for by-product ecological speciation? |author=R. Cruz, M. Carballo, P. Conde-Padín, and E. Rolán-Alvarez |journal=Journal of Evolutionary Biology |year=2004 |volume=17 |issue=2 |pages=288–293 |doi=10.1111/j.1420-9101.2003.00689.x |pmid=15009262 |s2cid=23589841 |url=https://onlinelibrary.wiley.com/doi/epdf/10.1111/j.1420-9101.2003.00689.x }} Both marine and freshwater stickleback fish have shown strong evidence of having speciated this way.{{Citation|title=Evidence for ecology's role in speciation |author=Jeffrey S McKinnon, Seiichi Mori, Benjamin K Blackman, Lior David, David M Kingsley, Leia Jamieson, Jennifer Chou, and Dolph Schluter |journal=Nature |year=2004 |volume=429 |issue=6989 |pages=294–298 |doi=10.1038/nature02556 |pmid=15152252 |bibcode=2004Natur.429..294M |s2cid=2744267 }}{{Citation|title=Divergent sexual selection enhances reproductive isolation in sticklebacks |author=J W Boughman |journal=Nature |year=2001 |volume=411 |issue=6840 |pages=944–948 |doi=10.1038/35082064 |pmid=11418857 |bibcode=2001Natur.411..944B |s2cid=5669795 }}{{Citation|title=Natural selection and parallel speciation in sympatric sticklebacks |author=Howard. D. Rundle, L. Nagel, J. Wenrick Boughman, and D. Schluter |journal=Science |year=2000 |volume=287 |issue=5451 |pages=306–308 |doi=10.1126/science.287.5451.306 |pmid=10634785 |bibcode=2000Sci...287..306R |s2cid=7696251 }}{{Citation|title=Body Size, Natural Selection, and Speciation in Sticklebacks |author=Laura Nagel and Dolph Schluter |journal=Evolution |year=1998 |volume=52 |issue=1 |pages=209–218 |doi=10.1111/j.1558-5646.1998.tb05154.x |pmid=28568156 |s2cid=37489257 |doi-access=free }} Evidence is also found in Neochlamisus bebbianae leaf beetles, Timema cristinae walking-stick insects,{{Citation|title=Host-plant adaptation drives the parallel evolution of reproductive isolation |author=Patrik Nosil, Bernard J Crespi, and Cristina P Sandoval |journal=Nature |year=2002 |volume=417 |issue=6887 |pages=440–443 |doi=10.1038/417440a |pmid=12024213|bibcode=2002Natur.417..440N |s2cid=4421774 }}{{Citation|title=Reproductive isolation driven by the combined effects of ecological adaptation and reinforcement |author=P Nosil, B J Crespi, and C 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 }} and in the butterfly species Heliconius melpomene and H. cydno which are thought to have diverged recently due to assortive mating being enhanced where the species populations meet in sympatry.{{Citation|title=Reproductive isolation caused by colour pattern mimicry |author=Chris D. Jiggins, Russell E. Naisbit, Rebecca L. Coe and James Mallet |journal=Nature |year=2001 |volume=411 |issue=6835 |pages=302–305 |doi=10.1038/35077075 |pmid=11357131 |bibcode=2001Natur.411..302J |s2cid=2346396 |url=http://doc.rero.ch/record/7889/files/Jiggins_Chris_D._-_Reproductive_isolation_caused_by_coulour_20070615.pdf }}

Angiosperms (flowering plants) require some form of pollination—many of which require another animal to transfer pollen from one flower to another.{{cite book | last = Abrol | first = Dharam P. | title = Pollination Biology | name-list-style = vanc |year=2012 |chapter=Non Bee Pollinators-Plant Interaction |volume=Chapter 9 |pages=265–310 |doi=10.1007/978-94-007-1942-2_9|isbn=978-94-007-1941-5 }} Biotic pollination methods require pollinators such as insects (e.g. bees, butterflies, moths, wasps, beetles, and other invertebrates), birds, bats,{{Cite journal |last1=Stewart |first1=Alyssa B. |last2=Dudash |first2=Michele R. |date=2018-01-01 |title=Foraging strategies of generalist and specialist Old World nectar bats in response to temporally variable floral resources |journal=Biotropica |volume=50 |issue=1 |pages=98–105 |doi=10.1111/btp.12492|bibcode=2018Biotr..50...98S |s2cid=90515964 }} and other vertebrate species. Because of this evolutionary relationship between pollinators and pollen-producing plants, plants and animals become mutually dependent on each other—the pollinator receives food in the form of nectar and the flower gains the ability to propagate its genes.

In the event that an animal uses a different pollination source, plants can become reproductively isolated.{{rp|193}} Pollinator isolation is a specific form of sexual isolation. The botanist Verne Grant distinguished between two types of pollinator isolation: mechanical isolation and ethological isolation.{{rp|193}}{{Citation|title=Plant Speciation |author=Verne Grant |date=1971 |publisher=Columbia University Press |location=New York |isbn=978-0231083263 |pages=432 }}{{rp|75}}

File:Eulaema cingulata with Catasetum saccatum and Catasetum discolor pollen atttachment locations.png

Mechanical isolation results from anatomical differences of a flower or pollinator preventing pollination from occurring. For example, in the bee Eulaema cingulata, pollen from Catasetum discolor and C. saccatum is attached to different parts of the body (ventrally and dorsally respectively).{{rp|194}}{{Citation|title=Pollination by Euglossine Bees |author=Robert L. Dressler |journal=Evolution |year=1968 |volume=22 |issue=1 |pages=202–210 |doi=10.2307/2406664 |jstor=2406664 |pmid=28564982 |url=https://onlinelibrary.wiley.com/doi/pdf/10.1111/j.1558-5646.1968.tb03463.x }} Another example is with elephant's head and little elephant's head plants. They are not known to hybridize despite growing in the same region and being pollinated by the same bee species. Pollen is attached to different parts of the bee rendering the flowers isolated. Mechanical isolation also includes pollinators who are unable to pollinate due to physical inabilities.{{rp|194}} Nectar spur length, for example, could vary in size in a flower species resulting in pollination from different lepidopteran species due to the lengths preventing body contact with the flower's pollen.

File:Differential flower visitiation by pollinators - Graph.svg

Ethological isolation is based on behavioral traits of pollinators that prefer different morphological characteristics of a flower either genetically or through learned behavior. These characteristics could be the overall shape and structure, color, type of nectar, or smell of the flower.{{rp|194}} In some cases, mutualisms evolve between a pollinator and its host, cospeciating with near-congruent, parallel phylogenies.{{rp|196}} That is, the dependent relationship results in closely identical evolutionary trees indicating that speciation events and the rate of speciation is identical. Examples are found in fig wasps and their fig hosts, with each fig wasp species pollinating a specific fig species.{{Citation|title=Female figs as traps: Their impact on the dynamics of an experimental fig tree-pollinator-parasitoid community |author=Nazia Suleman, Steve Sait, and Stephen G.Compton |journal=Acta Oecologica |year=2015 |volume=62 |pages=1–9 |doi=10.1016/j.actao.2014.11.001 |bibcode=2015AcO....62....1S |url= http://eprints.whiterose.ac.uk/85568/7/Female%20plants%20as%20traps%20paper%20%283%29.pdf}} The yucca and yucca moth exhibit this same pattern.{{cite journal |last1=Pellmyr |first1=Olle |last2=Thompson |first2=John N. |last3=Brown |first3=Johnathan M. |last4=Harrison |first4=Richard G. |date=1996 |title=Evolution of pollination and mutualism in the yucca moth lineage |journal=American Naturalist |volume=148 |issue=5 |pages=827–847 |doi=10.1086/285958 |jstor=2463408 |s2cid=84816447 }}

Image:Aquilegia pubescens-formosa hybrid-swarm flowers close h.jpg

File:Flower color and nectar volume as a function of pollinator species ranges.svg

In a striking case, two closely related flowering plants (Erythranthe lewisii and E. cardinalis) have speciated due to pollinator isolation in complete sympatry (speciation occurring without any physical, geographic isolation). E. lewisii has changed significantly from its sister species in that its evolved pink flowers, broad petals, shorter stamens (the pollen-producing part of the plant), and a lower volume of nectar. It is entirely pollinated by bees with almost no crossing in nature. E. cardinalis is pollinated by hummingbirds and exhibits red, tube-shaped flowers, larger stamens, and a lot of nectar. It is thought that nectar volume as well as a genetic component (an allele substitution that controls color variation) maintains isolation.{{Citation|title=Allele substitution at a flower colour locus produces a pollinator shift in monkeyflowers |author=H. D. Bradshaw Jr and Douglas W. Schemske |journal=Nature |year=2003 |volume=426 |issue=6963 |pages=176–178 |doi=10.1038/nature02106 |pmid=14614505 |bibcode=2003Natur.426..176B |s2cid=4350778 }}{{Citation|title=Components of Reproductive Isolation Between the Monkeyflowers Mimulus lewisii and M. cardinalis (Phrymaceae) |author=Justin Ramsey, H. D. Bradshaw, and Douglas W. Schemske |journal=Evolution |year=2003 |volume=57 |issue=7 |pages=1520–1534 |doi=10.1554/01-352 |pmid= 12940357|s2cid=198156112 }} A similar pattern has been found in Aquilegia pubescens and A. formosa. In this species pair, A. pubescens is pollinated by hawkmoths while A. formosa is pollinated by hummingbirds.{{rp|197}} Unlike in Erythranthe, these species reside in different habitats but exhibit hybrid forms where their habitats overlap;{{Citation|title=Floral and Ecological Isolation Between Aquilegia formosa and Aquilegia pubescens |author=Scott A. Hodges and Michael L. Arnold |journal=Proceedings of the National Academy of Sciences |year=1994 |volume=91 |issue=7 |pages=2493–2496 |doi=10.1073/pnas.91.7.2493 |pmid=8146145 |pmc=43395 |bibcode=1994PNAS...91.2493H |url=https://www.pnas.org/content/pnas/91/7/2493.full.pdf |doi-access=free }} though they remain separate species suggesting that the hybrid flowers may be less attractive to their pollinator hosts.{{rp|197}}

Four geographic-based scenarios involving pollinator isolation are known to occur:

• The most common framework for pollinator isolation in a geographic context implies that floral trait divergence occurs as a result of geographic isolation (allopatrically). From there, a population has the potential to encounter different pollinators ultimately resulting in selection favoring traits to attract the pollinators and achieve reproductive success.{{rp|198}}
• Another scenario involves an initial allopatric stage, wherein secondary contact occurs at a variable level of reproductive isolation—high isolation is effectively allopatric speciation whereas low isolation is effectively sympatric. This "two-stage" model is indicated in the three-spined sticklebacks{{Citation|title=Reproductive character displacement of male stickleback mate preference: reinforcement or direct selection? |author=A Y K Albert and D Schluter |journal=Evolution |year=2004 |volume=58 |issue=5 |pages=1099–1107 |doi=10.1111/j.0014-3820.2004.tb00443.x |pmid=15212390|s2cid=13882516 |doi-access=free }} as well as the apple maggot fly and its apple hosts.{{Citation|title=Allopatric genetic origins for sympatric host-plant shifts and race formation in Rhagoletis |author=Jeffrey L Feder, Stewart H Berlocher, Joseph B Roethele, Hattie Dambroski, James J Smith, William L Perry, Vesna Gavrilovic, Kenneth E Filchak, Juan Rull, and Martin Aluja |journal=Proceedings of the National Academy of Sciences of the United States of America |year=2003 |volume=100 |issue=18 |pages=10314–10319 |doi=10.1073/pnas.1730757100 |pmid=12928500 |pmc=193558 |bibcode=2003PNAS..10010314F |doi-access=free }}
• A pollinator can change preferences due to its own evolution driving selection to favor traits that align with the pollinators changed preferences.{{rp|198}}
• There exists the possibility that when two populations become isolated geographically, a plant or pollinator could go extinct in one of the populations driving selection to favor different traits.{{Citation|title=Pollination Biology of Nemophila menziesii (Hydrophyllaceae) with Comments on the Evolution of Oligolectic Bees |author=Robert William Cruden |journal=Evolution |year=1972 |volume=26 |issue=3 |pages=373–389 |doi=10.1111/j.1558-5646.1972.tb01943.x |pmid=28563062 |s2cid=39629939 |doi-access=free }}

File:Ecological Speciation (pollinator isolation) Schematic-2.svg or parapatry. Novel pollinators drive the selection of new traits (purple petals) in the isolated populations eventually leading to speciation of the flower populations. It is possible for the same pollinator to drive the selection of new flower traits as long as the proportions of pollinators differ enough.]]

Jerry Coyne and H. Allen Orr contend that any scenario of pollinator isolation in allopatry demands that incipient stages should be found in different populations. This has been observed to varying degrees in several species-pollinator pairs. Flower size of Raphanus sativus (in this case, wild radish in 32 California populations) has been found to differ in accordance with larger honeybee pollinators.{{cite book |last1=Mazer |first1=Susan J. |last2=Meade |first2=Daniel E. |editor-last1=Mousseau |editor-first1=Timothy A. |editor-last2=Sinervo |editor-first2=Barry |editor-last3=Endler |editor-first3=John |title=Adaptive Genetic Variation in the Wild |publisher=Oxford University Press |date=2000 |pages=157–186 |chapter=Chapter 7: Geographic Variation in Flower Size in Wild Radish: The Potential Role of Pollinators in Population Differentiation |isbn=978-0195121834 |name-list-style=amp}} Polemonium viscosum flowers have been found to increase in size along an alpine gradient in the Colorado Rocky Mountains as flies pollinate at the timberline whereas bumblebees pollinate at higher elevations.{{Citation|title=Measuring Pollinator-Mediated Selection on Morphometric Floral Traits: Bumblebees and the Alpine Sky Pilot, Polemonium viscosum |author=Candace Galen |journal=Evolution |year=1989 |volume=43 |issue=4 |pages=882–890 |doi=10.2307/2409315 |jstor=2409315 |pmid= 28564200}} A similar pattern involving the timing in which hawkmoths (Hyles lineata) are active is documented in three subspecies of Aquilegia coerulea, the Rocky Mountain columbine found across the western United States.{{Citation|title=Hawkmoths and the Geographic Patterns of Floral Variation in Aquilegia caerulea |author=Russell B. Miller |journal=Evolution |year=1981 |volume=35 |issue=4 |pages=763–774 |doi=10.1111/j.1558-5646.1981.tb04936.x |pmid=28563131 |s2cid=38127528 |doi-access=free }}

The most notable example according to Coyne and Orr is that of the African orchid subspecies Satyrium hallackii hallackii and Satyrium hallackii ocellatum.{{rp|199–200}} The latter is pollinated by moths and exhibits long nectar spurs that correlate with the moth's proboscis. Unlike the inland, grassland habitat of subspecies hallackii, ocellatum resides in coastal populations and has short spurs that correlate with its primary carpenter bee pollinator. The moths are unable to find suitable nest sites in coastal habitats while the bees are unable inland. This pattern separates the pollinator populations but does not separate the orchid population driving selection to favor flower differences that better-match the local pollinators.{{Citation|title=Pollination ecotypes of Satyrium hallackii (Orchidaceae) in South Africa |author=S. D. Johnson |journal=Botanical Journal of the Linnean Society |year=1997 |volume=123 |issue=3 |pages=225–235 |doi=10.1111/j.1095-8339.1997.tb01415.x |doi-access=free }} A similar pattern has been detected in studies of the Disa draconis complex in South Africa.{{Citation|title=Long-Tongued Fly Pollination and Evolution of Floral Spur Length in the Disa draconis Complex (Orchidaceae) |author=S. D. Johnson and K. E. Steiner |journal=Evolution |year=1997 |volume=51 |issue=1 |pages=45–53 |doi=10.1111/j.1558-5646.1997.tb02387.x |pmid=28568792 |s2cid=43420068 |doi-access= }}

{{Main|Allochronic speciation}}

File:Allochronic speciation.svg

Temporal isolation is based on the reduction of gene flow between two populations due to different breeding times (phenology). It is also referred to as allochronic isolation, allochronic speciation, or allochrony. In plants, breeding in regards to time could involve the receptivity of stigma to accepting sperm, periods of pollen release (such as in conifer trees where cones disperse pollen via wind), or overall timing of flowering. In contrast, animals often have mating periods or seasons (and many aquatic animals have spawning times).{{rp|202}} Migratory patterns have also been implicated in allochronic speciation.{{Citation|title=The Role of Seasonal Migration in Population Divergence and Reproductive Isolation |author=Sheela P. Turbek, Elizabeth S.C. Scordato, and Rebecca J. Safran |journal=Trends in Ecology & Evolution |year=2018 |volume=33 |issue=3 |pages=164–175 |doi=10.1016/j.tree.2017.11.008 |pmid= 29289354 |doi-access=free }}{{Citation|title=Spatial Isolation and Temporal Variation in Fitness and Condition Facilitate Divergence in a Migratory Divide |author=Claudia Hermes, Raeann Mettler, Diego Santiago-Alarcon, Gernot Segelbacher, and H. Martin Schaefer |journal=PLOS ONE |year=2015 |volume=10 |issue=12 |pages= e0144264|doi=10.1371/journal.pone.0144264 |pmid=26656955 |pmc=4681481 |bibcode=2015PLoSO..1044264H |doi-access=free }}{{Citation |title=Speciation in Birds | author=Trevor Price |date=2008 |pages=1–64 |publisher=Roberts and Company Publishers | isbn=978-0-9747077-8-5 }}{{rp|92–96}}

For allochronic speciation to be considered to have actually occurred, the model necessitates three major requirements:{{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 }}

1. Phylogenetic analysis indicates the incipient species are sister taxa
2. Breeding timing is genetically-based (heritable to offspring)
3. The source of divergence is explicitly allochrony and not the result of reinforcement or other mechanisms

Allochrony is thought to evolve more easily the greater the heritability of reproductive timing—that is, the greater the link between genes and the timing of reproduction—the more likely speciation will occur.{{Citation|title=Population structure attributable to reproductive time: isolation by time and adaptation by time |author=Andrew P Hendry and Troy Day |journal=Molecular Ecology |year=2005 |volume=14 |issue=4 |pages=901–916 |doi=10.1111/j.1365-294X.2005.02480.x |pmid=15773924 |s2cid=8226535 |doi-access=free |bibcode=2005MolEc..14..901H }} Temporal isolation is unique in that it can be explicitly sympatric as well as nongenetic;{{rp|203}} however genetic factors must be involved for isolation to lead to complete reproductive isolation and subsequent speciation. Speciation by allochrony is known to occur in three time frames: yearly (e.g. periodic cicadas emerging over decades or multi-decadal bamboo flowerings), seasonal (organisms that breed during times of the year such as winter or summer), and daily (e.g. daily spawning times of corals). The table list below summarizes a number of studies considered to be strong or compelling examples of allochronic speciation occurring in nature.

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Selection against migrants, or immigrant inviability, is hypothesized to be a form of ecological isolation. This type of speciation involves the low survival rates of migrants between populations because of their lack of adaptations to non-native habitats. There is little understanding the relationship between post-mating, pre-zygotic isolation and ecology. Post-mating isolation occurs between the process of copulation (or pollination) and fertilization—also known as gametic isolation.{{rp|232}} Some studies involving gametic isolation in Drosophila fruit flies,{{Citation|title=Cryptic reproductive isolation in the Drosophila simulans species complex |author=Catherine S. C. Price, Christine H. Kim, Carina J. Gronlund, and Jerry A. Coyne |journal=Evolution |year=2001 |volume=55 |issue=1 |pages=81–92 |doi=10.1111/j.0014-3820.2001.tb01274.x |pmid=11263748 |s2cid=18100324 |doi-access=free }} ground crickets,{{Citation|title=Conspecific Sperm Precedence is an Effective Barrier to Hybridization Between Closely Related Species |author=Daniel J. Howard, Pamela G. Gregory, Jiming Chu, and Michael L. Cain |journal=Evolution |year=1998 |volume=52 |issue=2 |pages=511–516 |doi=10.1111/j.1558-5646.1998.tb01650.x |pmid=28568320 |s2cid=8184734 |doi-access=free }} and Helianthus plants{{Citation|title=Interspecific Pollen Competition as a Reproductive Barrier Between Sympatric Species of Helianthus (Asteraceae) |author=Loren H. Rieseberg, Andree M. Desrochers and Sue J. Youn |journal=American Journal of Botany |year=1995 |volume=82 |issue=4 |pages=515–519 |doi=10.2307/2445699 |jstor=2445699 }} suggest that there may be a role in ecology; however it is undetermined.

[[File:Post-Zygotic Ecological Isolation.svg|right|thumb|upright=1.5|Three forms of ecologically-based post-zygotic isolation:

1. Ecologically-independent post-zygotic isolation.

2. Ecologically-dependent post-zygotic isolation.

3. Selection against hybrids.]]

Ecologically-independent post-zygotic isolation arises out of genetic incompatibilities between two hybrid individuals of a species.{{Citation|title=A Genetic Interpretation of Ecologically Dependent Isolation |author=Howard D. Rundle Michael C. Whitlock |journal=Evolution |year=2001 |volume=55 |issue=1 |pages=198–201 |doi=10.1111/j.0014-3820.2001.tb01284.x |pmid=11263739 |s2cid=14710367 |doi-access=free }} It is thought that in some cases, hybrids have lower fitness especially based on the environment in which they reside. For example, in extreme environments with limited ecological niches to exploit, high fitness is necessitated, whereas if an environment has lots of niches, lower fit individuals may be able to survive for longer. Some studies indicate that these incompatibilities are a cause of ecological speciation because they can evolve quickly through divergent selection.

Ecologically-dependent post-zygotic isolation results from reduced hybrid fitness due to its position in an ecological niche—that is, parental species occupy slightly different niches, but their hybrid offspring end up requiring a niche that is a blend between the two of which does not typically exist (in regard to a fitness landscape). This has been detected in populations of sticklebacks (Gasterosteus aculeatus),{{Citation|title=A test of ecologically dependent postmating isolation between sympatric sticklebacks |author=Howard D Rundle |journal=Evolution |year=2002 |volume=56 |issue=2 |pages=322–329 |doi=10.1111/j.0014-3820.2002.tb01342.x |pmid=11926500 |s2cid=11550301 |doi-access=free }}{{Citation|title=Ecological Speciation in Sticklebacks: Environment-Dependent Hybrid Fitness |author=Todd Hatfield and Dolph Schluter |journal=Evolution |year=1999 |volume=53 |issue=3 |pages=866–873 |doi=10.1111/j.1558-5646.1999.tb05380.x |pmid=28565618 |s2cid=10638478 |doi-access=free }} water-lily beetles (Galerucella nymphaeae),{{Citation|title=Genetically based polymorphisms in morphology and life history associated with putative host races of the water lily leaf beetle, Galerucella nymphaeae |author=Stephanie M Pappers, Gerard van der Velde, N Joop Ouborg, and Jan M van Groenendael |journal=Evolution |year=2002 |volume=56 |issue=8 |pages=1610–1621 |doi=10.1111/j.0014-3820.2002.tb01473.x |pmid=12353754 |s2cid=23891554 }} pea aphids,{{Citation|title=Reproductive isolation between divergent races of pea aphids on two hosts. II. Selection against migrants and hybrids in the parental environments |author=Sara Via, A. C. Bouck, and S. Skillman |journal=Evolution |year=2000 |volume=54 |issue=5 |pages=1626–1637 |doi=10.1111/j.0014-3820.2000.tb00707.x |pmid=11108590 |s2cid=26339284 |doi-access=free }} and tephritid flies (Eurosta solidaginis).{{Citation|title=Hybridization Studies on the Host Races of Eurosta Solidaginis: Implications for Sympatric Speciation |author=Timothy P Craig, John D Horner, and Joanne K Itami |journal=Evolution |year=1997 |volume=51 |issue=5 |pages=1552–1560 |doi=10.1111/j.1558-5646.1997.tb01478.x |pmid=28568625 |s2cid=6447741 |doi-access=free }}

Selection against hybrids can sometimes (it is possible that nonecological speciation can be attributed) be considered a form of ecological isolation if it originates from an ecological mechanism. For example, the hybrid offspring may be seen as "less attractive" to mates due to intermediate sexual displays or differences in sexual communication. The end result is that the genes of each parental population are unable to intermix as they are carried by a hybrid who is unlikely to reproduce. This pattern of sexual selection against hybrid offspring has been found in Heliconius butterflies. The two species H. cydno and H. melpomene are distributed sympatrically in South America and hybridize infrequently.{{Citation|title=Disruptive sexual selection against hybrids contributes to speciation between Heliconius cydno and Heliconius melpomene |author=R. E. Naisbit, C. D. Jiggins, and J. Mallet |journal=Proceedings of the Royal Society B: Biological Sciences |year=2001 |volume=268 |issue=1478 |pages=1849–1854 |doi=10.1098/rspb.2001.1753 |pmid=11522205 |pmc=1088818 }} When they do hybridize, the species shows strong assortive mating due to the mimicry-evolved color pattern that hybrid offspring have an intermediate of. Similar patterns have been found in lacewings{{cite book |last1=Wells |first1=Marta Martínez |last2=Henry |first2=Charles |editor-last1=Howard |editor-first1=Daniel J. |editor-last2=Berlocher |editor-first2=Stewart H. |title=Endless Forms: Species and Speciation |publisher=Oxford University Press |date=1998 |pages=217–233 |chapter=Songs, reproductive isolation and speciation in cryptic species of insects: a case study using green lacewings |isbn=978-0195109016 |name-list-style=amp}} migrating patterns of Sylvia atricapilla bird populations,{{Citation|title=SE- and SW-migrating Blackcap (Sylvia atricapilla) populations in Central Europe: Orientation of birds in the contact zone |author=Andreas J. Helbig |journal=Journal of Evolutionary Biology |year=1991 |volume=4 |issue=4 |pages=657–670 |doi=10.1046/j.1420-9101.1991.4040657.x |s2cid=84847304 |doi-access=free }} wolf spiders (Schizocosa ocreata and S. rovneri) and their courtship behaviors,{{Citation|title=The Inheritance of Courtship Behavior and its Role as a Reproductive Isolating Mechanism in Two Species of Schizocosa Wolf Spiders (Araneae; Lycosidae) |author=Gail E. Stratton and George W. Uetz |journal=Evolution |year=1986 |volume=40 |issue=1 |pages=129–141 |doi=10.1111/j.1558-5646.1986.tb05724.x |pmid=28564117 |s2cid=7755906 |doi-access=free }} sympatric benthic and limnetic sticklebacks (the Gasterosteus aculeatus complex),{{Citation|title=Sexual Selection Against Hybrids Between Sympatric Stickleback Species: Evidence from a Field Experiment |author=Steven M Vamosi and Dolph Schluter |journal=Evolution |year=1999 |volume=53 |issue=8 |pages=874–879 |doi=10.1111/j.1558-5646.1999.tb05381.x |pmid=28565643 |s2cid=205781377 |doi-access=free }} and the Panamanian butterflies Anartia fatima and A. amathea.{{Citation|title=Speciation in two neotropical butterflies: extending Haldane's rule |author=N. Davies, A. Aiello, J. Mallet, A. Pomiankowski, and R. E. Silberglied |journal=Proceedings of the Royal Society B: Biological Sciences |year=1997 |volume=264 |issue=1383 |pages=845–851 |doi=10.1098/rspb.1997.0118 |pmc=1688429 |bibcode=1997RSPSB.264..845D }} Flowers involving pollinator discrimination against hybrids have shown this pattern as well, in monkey flowers (Erythranthe lewisii and Erythranthe cardinalis){{Citation|title=Pollinator preference and the evolution of floral traits in monkeyflowers (Mimulus) |author=Douglas W. Schemske and H. D. Bradshaw Jr. |journal=Proceedings of the National Academy of Sciences |year=1999 |volume=96 |issue=21 |pages=11910–11915 |doi=10.1073/pnas.96.21.11910 |pmid=10518550 |pmc=18386 |bibcode=1999PNAS...9611910S |url=https://www.pnas.org/content/pnas/96/21/11910.full.pdf |doi-access=free }} and in two species of the Louisiana iris group, Iris fulva and I. hexagona.{{Citation|title=Site-to-site differences in pollinator visitation patterns in a Louisiana iris hybrid zone |author=Simon K. Emms and Michael L. Arnold |journal=Oikos |year=2000 |volume=91 |issue=3 |pages=568–578 |doi=10.1034/j.1600-0706.2000.910319.x }}

• Laboratory experiments of speciation

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Category:Speciation

Category:Ecology