Allopatric speciation

Allopatric speciation (from the ancient Greek allos, meaning "other", and patris, meaning "fatherland"), also referred to as geographic speciation, vicariant speciation, or its earlier name, the dumbbell model,[1] is a mode of speciation that occurs when biological populations of the same species become isolated from each other to an extent that prevents or interferes with genetic interchange.

Various geographic changes can arise such as the movement of continents, and the formation of mountains, islands, bodies of water, or glaciers. Human activity such as agriculture or developments can also change the distribution of species populations. These factors can substantially alter a regions geography, resulting in the separation of a species population into isolated subpopulations. The vicariant populations then undergo genetic changes as they become subjected to different selective pressures, experience genetic drift, and accumulate different mutations in the separated populations gene pools. The barriers prevent the exchange of genetic information between the two populations leading to reproductive isolation. If the two populations come into contact they will be unable to reproduce—effectively speciating. Other isolating factors such as population dispersal leading to emigration can cause speciation (e.g. the dispersal and isolation of a species on an oceanic island) and is considered a special case of allopatric speciation called peripatric speciation.

Allopatric speciation is typically subdivided into two major models: vicariance and peripatric. Both models differ from one another by virtue of their population sizes and geographic isolating mechanisms. The terms allopatric, allopatry, and vicariant are often used in biogeography to describe the relationship between organisms whose ranges do not significantly overlap but are immediately adjacent to each other—they do not occur together except in a narrow contact zone. Historically, the language used to refer to modes of speciation directly reflected biogeographical distributions.[2] As such, allopatry is a geographical distribution opposed to sympatry (speciation within the same area). Furthermore, the terms allopatric, vicariant, and geographical speciation are often used interchangeably in the scientific literature.[2] This article will follow a similar theme, with the exception of special cases such as peripatric, centrifugal, among others.

Observation of nature creates difficulties in witnessing allopatric speciation from "start-to-finish" as it operates as a dynamic process.[3] From this arises a host of various issues in defining species, defining isolating barriers, measuring reproductive isolation, among others.[4] Nevertheless, verbal and mathematical models, laboratory experiments, and empirical evidence overwhelmingly supports the occurrence of allopatric speciation in nature.[1][5] Mathematical modeling of the genetic basis of reproductive isolation supports the plausibility of allopatric speciation; whereas laboratory experiments of Drosophila and other animal and plant species have confirmed that reproductive isolation evolves as a byproduct of natural selection.[1]

Vicariance model

Figure 2a: A species population becomes separated by a geographic barrier, whereby reproductive isolation evolves producing two separate species.

Speciation by vicariance is widely regarded as the most common form of speciation;[5] and is the primary model of allopatric speciation. Vicariance is a process by which the geographical range of an individual taxon, or a whole biota, is split into discontinuous populations (disjunct distributions) by the formation of an extrinsic barrier to the exchange of genes: that is, a barrier arising externally to a species. These extrinsic barriers often arise from various geologic-caused, topographic changes such as: the formation of mountains (orogeny); the formation of rivers or bodies of water; glaciation; the formation or elimination of land bridges; the movement of continents over time (by tectonic plates); or island formation and can change the distribution of species populations. The emergence of suitable or unsuitable habitat configurations may arise from these changes and can originate by changes in climate or even large scale human activities (for example, agricultural, civil engineering developments, and habitat fragmentation). Among others, these many factors can alter a regions geography in substantial ways, resulting in the separation of a species population into isolated subpopulations. The vicariant populations then undergo genotypic or phenotypic divergence as: (a) they become subjected to different selective pressures, (b) they independently undergo genetic drift, and (c) different mutations arise in the gene pools of the populations. The extrinsic barriers prevent the exchange of genetic information between the two populations, inevitably leading to to differentiation due to the ecologically different habitats they experience; whereby selective pressure invariably leads to complete reproductive isolation.[1] (See figure 2a). Furthermore, a species' proclivity to remain in its ecological niche (see phylogenetic niche conservatism) through changing environmental conditions may also play a role in isolating populations from one another, driving the evolution of new lineages.[6][7]

Allopatric speciation can be represented as the extreme on a gene flow continuum. As such, the level of gene flow between populations in allopatry would be m=0, where m equals the rate of gene exchange. In sympatry m=0.5, while in parapatric speciation, 0 < m < 0.5 representing the entire continuum.[8] Some scientists reject this delineation due to its promulgation of the geographic mode classification scheme.[2][9] It also does not necessarily reflect the complex reality of speciation.[10] Allopatry is often regarded as the default or "null" model of speciation;[2][11] though debate exists as to whether this is a justified approach.[12]

Reproductive isolation

Reproductive isolation acts as the primary mechanism driving genetic divergence in allopatry[13] and can be amplified by divergent selection.[14] Pre-zygotic and post-zygotic isolation are often the most cited mechanisms for allopatric speciation, and as such, it is difficult to determine which form evolved first in an allopatric speciation event.[13] Pre-zygotic simply implies the presence of a barrier prior to any act of fertilization (e.g. an environmental barrier dividing two populations) while post-zygotic implies the prevention of successful inter-population crossing after fertilization (e.g. the production of an infertile hybrid). Since species pairs who diverged in allopatry often exhibit pre- and post-zygotic isolation mechanisms, investigation of the earliest stages in the life cycle of the species can indicate whether or not divergence occurred due to a pre-zygotic or post-zygotic factor. However, establishing the specific mechanism may not be accurate, as a species pair continually diverges over time. For example, if a plant experiences a chromosome duplication event, reproduction will occur, but sterile hybrids will result—functioning as a form of post-zygotic isolation. Subsequently, the newly-formed species pair may experience pre-zygotic barriers to reproduction as selection, acting on each species independently, will ultimately lead to genetic changes making hybrids impossible. From the researchers perspective, the current isolating mechanism may not reflect the past isolating mechanism.[13]

Reinforcement

Reinforcement has been a contentious factor in speciation and is more often invoked in sympatric speciation studies (as it requires the existence of some gene flow between two populations);[1] however, it is thought that reinforcement can also play a role in allopatric speciation—whereby the reproductive barrier is removed, reuniting the two previously isolated populations (see figure 2b). Upon secondary contact, individuals reproduce, creating low-fitness hybrids[15] (see figure 2b). Traits of the hybrids drive individuals to discriminate in mate choice, by which pre-zygotic isolation increases between the populations.[10] Some arguments have been put forth that suggest the hybrids themselves can possibly become their own species:[16] known as hybrid speciation). Reinforcement can play a role in all geographic modes (and other non-geographic modes) of speciation as long as gene flow is present and viable hybrids can be formed. The production of inviable hybrids is a form of reproductive character displacement, under which most definitions is the completion of a speciation event.[10]

Research has well established the fact that interspecific mate discrimination occurs to a greater extent between sympatric populations than it does in purely allopatric populations; however, other factors have been proposed to account for the observed patterns.[17] Reinforcement in allopatry has been shown to occur in nature, albeit with less frequency than a classic allopatric speciation event.[13] A major difficulty arises when interpreting reinforcement's role in allopatric speciation, as current phylogenetic patterns may suggest past gene flow. This masks possible initial divergence in allopatry and can indicate a "mixed-mode" speciation event—exhibiting both allopatric and sympatric speciation processes.[12]

Figure 2b: In allopatric speciation, a species population becomes separated by a geographic barrier, whereby reproductive isolation evolves producing two separate species. From this, if a recently separated population comes in contact again, low fitness hybrids may form, but reinforcement acts to complete the speciation process.

Mathematical models

Developed in the context of the genetic basis of reproductive isolation, mathematical scenarios model both prezygotic and postzygotic isolation with respect to the effects of genetic drift, selection, sexual selection, or various combinations of the three. Masatoshi Nei and colleagues were the first to develop a neutral, stochastic model of speciation by genetic drift alone. Both selection and drift can lead to postzygotic isolation, supporting the fact that two geographically separated populations can evolve reproductive isolation[1]—sometimes occurring rapidly.[18] Fisherian sexual selection can also lead to reproductive isolation if their are minor variations in selective pressures (such as predation risks or habitat differences) among each population.[19] (See the Further reading section below).

Further, mathematical models concerning reproductive isolation-by distance have shown that populations can experience increasing reproductive isolation that correlates directly with physical, geographical distance.[20][21] This has been exemplified in models of ring species;[10] however, it has been argued that ring species are a special case, representing reproductive isolation-by distance, but demonstrate parapatric speciation instead[1]—as parapatric speciation represents speciation occurring along a cline.

Other models

Various alternative models have been developed concerning allopatric speciation. Special cases of vicariant speciation have been studied in great detail, one of which is peripatric speciation, whereby a small subset of a species population becomes isolated geographically; and centrifugal speciation, an alternative model of peripatric speciation concerning expansion and contraction of a species range.[5] Other minor allopatric models have also been developed are are discussed below.

Peripatric

Peripatric speciation is a mode of speciation in which a new species is formed from an isolated peripheral population.[1] If a small population of a species becomes isolated (e.g. a population of birds on an oceanic island), selection can act on the population independent of the parent population. Given both geographic separation and enough time, speciation can result as a byproduct.[13]

In peripatric speciation, a small, isolated population on the periphery of a central population evolves reproductive isolation due to the reduction or elimination of gene flow between the two.

It can be distinguished from allopatric speciation by three important features: 1) the size of the isolated population, 2) the strong selection imposed by the dispersal and colonization into novel environments, and 3) the potential effects of genetic drift on small populations.[1] However, it can often be difficult for researchers to determine if peripatric speciation occurred as vicariant explanations can be invoked due to the fact that both models posit the absense of gene flow between the populations.[22]

The size of the isolated population is important because individuals colonizing a new habitat likely contain only a small sample of the genetic variation of the original population. This promotes divergence due to strong selective pressures, leading to the rapid fixation of an allele within the descendant population. This gives rise to the potential for genetic incompatibilities to evolve. These incompatibilities cause reproductive isolation, giving rise to rapid speciation events.[1]

Models of peripatry are supported mostly by species distribution patterns in nature. Oceanic islands and archipelagos provide the strongest empirical evidence that peripatric speciation occurs.[1]

Centrifugal

Centrifugal speciation is a variant, alternative model of peripatric speciation. This model contrasts with peripatric speciation by virtue of the origin of the genetic novelty that leads to reproductive isolation.[23] When a population of a species experiences a period of geographic range expansion and contraction, it may leave small, fragmented, peripherally isolated populations behind. These isolated populations will contain samples of the genetic variation from the larger parent population. This variation leads to a higher likelyhood of ecological niche specialization and the evolution of reproductive isolation.[5][24]

Centrifugal speciation has been largely ignored in the scientific literature.[25][23][26] Nevertheless, a wealth of evidence has been put forth by researchers in support of the model, much of which has not yet been refuted.[5] One example is the possible center of origin taking place within the Indo-West Pacific[25]

Microallopatric

Microallopatry refers to allopatric speciation occurring on a small geographic scale.[27] Examples of microallopatric speciation in nature have been described. Rico and Turner found intralacustrine allopatric divergence of Pseudotropheus callainos within Lake Malawi separated only by 35 meters.[28] Gustave Paulay found evidence that species in the subfamily Cryptorhynchinae have microallopatrically speciated on Rapa and its surrounding islets.[29] A sympatrically distributed triplet of diving beetle (Paroster) species living in aquifers of Australia's Yilgarn region have likely speciated microallopatrically within a 3.5 km2 area.[30]

The term was originally proposed by Hobart M. Smith to describe a level of geographic resolution. A sympatric population may exist in low resolution, whereas viewed with a higher resolution (i.e. on a small, localized scale within the population) it is "microallopatric".[31] Fitzpatrick et al. contends that this original definition, "is misleading because it confuses geographical and ecological concepts".[27]

Allopatric modes with secondary contact

Ecological allopatry

Ecological speciation can occur either in allopatrically, sympatrically, or parapatrically; the only requirement being that it occurs as a result of adaptation to different ecological or micro-ecological conditions.[32] Ecological allopatry is a reverse-ordered form of allopatric speciation in conjunction with reinforcement.[12] First, divergent selection separates a non-allopatric incipient species population emerging from pre-zygotic barriers, from which genetic differences evolve due to the obstruction of complete gene flow.[33]

Allo-parapatric and allo-sympatric

The terms allo-parapatric and allo-sympatric have been used to describe speciation scenarios where divergence occurs in in allopatry but speciation occurs only upon secondary contact.[1] These are effectively models of reinforcement[34] or "mixed-mode" speciation events.[12]

Observational evidence

Figure 3b: South America's areas of endemism.
Figure 3a: A cladogram of species in the Charis cleonus group superimposed over a map of South America showing the biogeographic ranges or each species.
Figure 3c: A hypothetical representation of species populations becoming isolated (blue and green) by the closure of the Isthmus of Panama (red circle). With the closure, North and South America became connected, allowing the exchange of species (purple). Grey arrows indicate the gradual movement of tectonic plates that resulted in the closure.
Figure 3d: The red shading indicates the range of the bonobo (Pan paniscus). The blue shading indicates the range of the Common chimpanzee (Pan troglodytes). This is an example of allopatric speciation because they are divided by a natural barrier (the Congo River) and have no habitat in common. Other Pan subspecies are shown as well.

As allopatric speciation is widely accepted as a common mode of speciation, the scientific literature is abundant with studies documenting its existence. The biologist Ernst Mayr was the first to summarize the contemporary literature of the time in 1942 and 1963. Many of the examples he set forth remain conclusive; however, modern research supports geographic speciation with molecular phylogenetics[35]—adding a level of robustness unavailable to early researchers.[1] The most recent thorough treatment of allopatric speciation (and speciation research in general is Jerry Coyne and H. Allen Orr's 2004 publication Speciation. They list six mainstream arguments that lend support to the concept of vicariant speciation:

Endemism

Islands are often home to species endemics—existing only on an island and nowhere else in the world—with nearly all taxa residing on isolated islands sharing common ancestry with a species on the nearest continent.[36] Not without challenge, there is typically a correlation between island endemics and diversity;[37] that is, that the greater the diversity (species richness) of an island, the greater the increase in endemism.[38] Increased diversity effectively drives speciation.[39] Furthermore, the number of endemics on an island is directly correlated with the relative isolation of the island and its area.[40] In some cases, speciation on islands has occurred rapidly.[41]

Dispersal and in situ speciation are the agents that explain the origins of the organisms in Hawaii.[42] Various geographic modes of speciation have been studied extensively in Hawaiian biota, and in particular, angiosperms appear to have speciated predominately in allopatric and parapatric modes.[42]

Islands are not the only geographic locations that have endemic species. South America has been studied extensively with its areas of endemism (see figure 3a) representing assemblages of allopatrically distributed species groups. Charis butterflies are a primary example (see figure 3b), confined to specific regions corresponding to phylogenies of other species of butterflies, amphibians, birds, marsupials, primates, reptiles, and rodents.[43] The pattern indicates repeated vicariant speciation events among these groups.[43] It is thought that rivers may play a role as the geographic barriers to Charis,[1] not unlike the river barrier hypothesis used to explain the high rates of diversity in the Amazon basin. Dispersal-mediated allopatric speciation is also thought to be a significant driver of diversification throughout the Neotropics.[44]

Adaptive radiations, like the Galapagos finches observed by Charles Darwin, is often a consequence of rapid allopatric speciation among populations. However, in the case of the finches of the Galapagos, among other island radiations such as the honeycreepers of Hawaii represent cases of limited geographic separation and were likely driven by ecological speciation.

Isthmus of Panama

Geological evidence supports the final closure of the isthmus of Panama approximately 2.7 to 3.5 mya,[45] with some evidence suggesting an earlier transient bridge existing between 13 to 15 mya.[46] Recent evidence increasingly points towards an older and more complex emergence of the Isthmus, with fossil and extant species dispersal (part of the American biotic interchange) occurring in three major pulses, to and from North and South America.[47] Further, the changes in terrestrial biotic distributions of both continents such as with Eciton army ants supports an earlier bridge or a series of bridges.[48][49] Regardless of the exact timing of the isthmus closer, biologists can study the species on the Pacific and Caribbean sides in what has been called, "one of the greatest natural experiments in evolution (see figure 3c)."[45] Additionally, as with most geologic events, the closure was unlikely to have occurred rapidly, but instead dynamically—a gradual shallowing of sea water over millions of years.[1]

Studies of snapping shrimp in the genus Alpheus have provided direct evidence of an allopatric speciation event,[50] as phylogenetic reconstructions support the relationships of 15 pairs of sister species pairs of Alpheus on each each side of the isthmus[45] and molecular clock dating supports their separation between 3 and 15 million years ago.[51] Recently diverged species reside in shallow mangrove waters[51] while older diverged species live in deeper water, correlating with a the gradual closure of the isthmus.[1] Further support of an allopatric divergence comes from laboratory experiments on the species pairs showing nearly complete reproductive isolation.[1]

Similar patterns of relatedness and distribution across the Pacific and Atlantic sides have been found in other species pairs such as:[52]

Refugia

Ice ages have played important roles in facilitating speciation among vertebrate species.[53] This concept of refugia has been applied to numerous groups of species and their biogeographic distributions.[1]

It has been found that many boreal forest birds speciated due to glaciation[53] and subsequent retreat, such as with North American sapsuckers (Yellow-bellied, Red-naped, and Red-breasted); the warbler's in the genus Setophaga (S. townsendii, S. occidentalis, and S. virens), Oreothlypis (O. virginiae, O. ridgwayi, and O. ruficapilla), and Oporornis (O. tolmiei and O. philadelphia now classified in the genus Geothlypis); Fox sparrow's (sub species P. (i.) unalaschensis, P. (i.) megarhyncha, and P. (i.) schistacea); Vireo (V. plumbeus, V. cassinii, and V. solitarius); flycatcher's (E. occidentalis and E. difficilis); chickadee's (P. rufescens and P. hudsonicus); and thrush's (C. bicknelli and C. minimus).[53]

As a special case of allopatric speciation, peripatric speciation is often invoked for instances of isolation in refugia (caused by glaciation) as small populations become isolated due to habitat fragmentation such as with North American red (Picea rubens) and black (Picea mariana) spruce [54] or the prairie dogs Cynomys mexicanus and Cynomys ludovicianus.[55]

Superspecies

Numerous species pairs or species groups show abutting distribution patterns, that is, reside in geographically distinct regions next to each other. They often share borders, many of which contain hybrid zones. Some examples of abutting species and superspecies (an informal rank referring to a complex of closely related allopatrically distributed species, also called allospecies[56]) include:

In birds, some areas are prone to high rates of superspecies formation (see speciation in birds) such as the 105 superspecies in Melanesia, comprising 66 percent of all bird species in the region.[60] Patagonia is home to 17 superspecies of forest birds,[61] while North America has 127 superspecies of both land and freshwater birds.[62] Sub-Saharan Africa has 486 passerine birds grouped into 169 superspecies.[63] Australia has numerous bird superspecies as well, with 34 percent of all bird species grouped into superspecies.[36]

Laboratory evidence

A simplification of an experiment where two vicariant lines of fruit flies were raised on harsh maltose and starch mediums respectively. The experiment was replicated with 8 populations; 4 with maltose and 4 with starch. Differences in adaptations were found for each population corresponding to the different mediums.[64] Later investigation found that the populations evolved behavioral isolation as a pleiotropic by-product from this adaptive divergence.[65] This form of pre-zygotic isolation is a prerequisite for speciation to occur.

Experiments on allopatric speciation are often complex and do not simply divide a species population into two. This is due to a host of defining parameters: measuring reproductive isolation, sample sizes (the number of matings conducted in reproductive isolation tests), bottlenecks, length of experiments, number of generations allowed,[66] or insufficient genetic diversity.[67] Various isolation indices have been developed to measure reproductive isolation (and are often employed in laboratory speciation studies) such as here (index Y [68] and index I [69]):

                              

Here, A and D represent the number of matings in heterogameticity where B and C represent homogametic matings. A and B is one population and D and C is the second population. A negative value of Y denotes negative assortive mating, a positive value denotes positive assortive mating (i. e. expressing reproductive isolation), and a null value (of zero) means the populations are experiencing random mating.[66]

The experimental evidence has solidly established the fact that reproductive isolation evolves as a by-product of selection.[1][14] Further, reproductive isolation has been shown to arise from pleiotropy (i.e. indirect selection acting on genes that code for more than one trait)—what has been referred to as genetic hitchhiking.[14] Limitations and controversies exist relating to whether laboratory experiments can accurately reflect the long-scale process of allopatric speciation that occurs in nature. Experiments often fall beneath 100 generations, far less than expected, as rates of speciation in nature are thought to be much larger.[1] Furthermore, rates specifically concerning the evolution of reproductive isolation in Drosophila are significantly higher than what is practiced in laboratory settings.[70] Using index Y presented previously, a survey of 25 allopatric speciation experiments (included in the table below) found that reproductive isolation was not as strong as typically maintained and that laboratory environments have not been well-suited for modeling allopatric speciation.[66] Nevertheless, numerous experiments have shown pre-zygotic and post-zygotic isolation in vicariance, some in less than 100 generations.[1]

Below is a non-exhaustive table of the laboratory experiments conducted on allopatric speciation. The first column indicates the species used in the referenced study, where the "Trait" column refers to the specific characteristic selected for or against in that species. The "Generations" column refers to the number of generations in each experiment performed. If more than one experiment was formed generations are separated by semicolons or dashes (given as a range). Some studies provide a duration in which the experiment was conducted. The "Mode" column indicates if the study modeled vicariant or peripatric speciation (this may not be explicitly. Direct selection refers to selection imposed to promote reproductive isolation whereas indirect selection implies isolation occurring as a pleiotropic byproduct of natural selection; whereas divergent selection implies deliberate selection of each allopatric population in opposite directions (e.g. one line with more bristles and the other line with less). Some studies performed experiments modeling or controlling for genetic drift. Reproductive isolation occurred pre-zygotically, post-zygotically, both, or not at all). It is important to note that many of the studies conducted contain multiple experiments within—a resolution of which this table does not reflect.

Laboratory studies of allopatric speciation[14][67][66][1]
Species Trait ~Generations (duration) Mode Selection type Studied Drift Reproductive isolation Reference Year
Drosophila
melanogaster		 Escape response 18 Vicariant Indirect; divergent Yes Pre-zygotic [71] 1969
Locomotion 112 Vicariant Indirect; divergent No Pre-zygotic [72] 1974
Temperature, humidity 70–130 Vicariant Indirect; divergent Yes Pre-zygotic [73] 1980
DDT adaptation 600 (25 years, +15 years) Vicariant Direct No Pre-zygotic [74] 2003
17, 9, 9, 1, 1, 7, 7, 7, 7 Direct, divergent Pre-zygotic [75] 1974
40; 50 Direct; divergent Pre-zygotic [76] 1974
Locomotion 45 Vicariant Direct; divergent No None [77][78] 1979
Direct; divergent Pre-zygotic [79] 1953
36; 31 Direct; divergent Pre-zygotic [80] 1956
EDTA adaptation 3 experiments, 25 each Semi-allopatric Indirect No Post-zygotic [81][82] 1966
8 experiments, 25 each Reinforcement Direct [83] 1997
Abdominal chaeta

number

 21-31 Vicariant Direct Yes None [84] 1958
Sternopleural chaeta number 32 Vicariant Direct No None [85] 1969
Phototaxis, geotaxis 20 Vicariant No None [86][87] 1975; 1981
Peripatric Yes [88] 1998
Vicariant; peripatric Yes [89] 1999
Direct; divergent Pre-zygotic [90][91][92][93] 1971; 1973; 1979; 1983
D. simulans Scutellar bristles, development speed, wing width;

desiccation resistance, fecundity, ethanol resistance;

courtship display, re-mating speed, lek behavior;

pupation height, clumped egg laying, general activity

 3 years Vicariant; peripatric Yes Post-zygotic [94] 1985
D. paulistorum 131; 131 Direct Pre-zygotic [95] 1976
5 years Vicariant [96] 1966
D. willistoni pH adaptation 34–122 Vicariant Indirect; divergent No Pre-zygotic [97] 1980
D. pseudoobscura Carbohydrate source 12 Vicariant Indirect Yes Pre-zygotic [65] 1989
Temperature adaptation 25–60 Vicariant Direct [98][99] 1964;

1969

Phototaxis, geotaxis 5–11 Vicariant Indirect No Pre-zygotic [100] 1966
Vicariant; peripatric Pre-zygotic [101][102] 1978; 1985
Peripatric; vicariant Yes [103] 1993
Temperature photoperiod; food 37 Vicariant Divergent Yes None [104] 2003
D.pseudoobscura &

D. persimilis

 22; 16; 9 Direct; divergent Pre-zygotic [105] 1950
4 experiments, 18 each Direct Pre-zygotic [106] 1966
D. mojavensis 12 Direct Pre-zygotic [107] 1987
Development time 13 Divergent Yes None [108] 1998
D. adiastola Peripatric Yes Pre-zygotic [109] 1974
D. silvestris Peripatric Yes [110] 1980
Musca domestica Geotaxis 38 Vicariant Indirect No Pre-zygotic [111] 1974
Geotaxis 16 Vicariant Direct; divergent No Pre-zygotic [112] 1975
Peripatric Yes [113] 1991
Bactrocera cucurbitae Development time 40–51 Divergent Yes Pre-zygotic [114] 1999
Zea mays 6; 6 Direct; divergent Pre-zygotic [115] 1969
D. grimshawi Peripatric [116]

History and research techniques

Early speciation research typically reflected geographic distributions and were thus termed geographic, semi-geographic, and non-geographic.[2] Geographic speciation corresponds to todays usage of the term allopatric speciation, and in 1869, Moritz Wagner was the first to propose the concept[117] of which he used the term 'Seperationstheorie'.[118] His idea was later interpreted by Ernst Mayr as a form of founder effect speciation as it focused primarily on small geographically isolated populations[118] (see peripatric speciation).

Edward Bagnall Poulton, an evolutionary biologist and strong proponent of the importance of natural selection was the first to highlight the role of geographic isolation in promoting speciation;[10] in the process coining the term "sympatric speciation" in 1903.[119]

Controversy exists as to whether Charles Darwin recognized a true geographical-based model of speciation in his publication of the Origin of Species.[118] F. J. Sulloway contends that his position on speciation was "misleading" at the most[120] and may have later misinformed Wagner and David Starr Jordan into believing that Darwin viewed sympatric speciation as the most important mode of speciation.[1] Nevertheless, Darwin never fully accepted Wagner's concept of geographical speciation.[118]

Ernst Mayr in 1994

David Starr Jordan played a significant role in promoting allopatric speciation in the early 20th century, providing a wealth of evidence from nature to support the theory.[1][117][121] Much later, the biologist Ernst Mayr was the first to encapsulate the then contemporary literature in his 1942 publication Systematics and the Origin of Species, from the Viewpoint of a Zoologist and in his subsequent 1963 publication Animal Species and Evolution. Like Jordan's works, they relied on direct observations of nature, documenting the occurrence of allopatric speciation, of which is widely accepted today.[1] Prior to this research, Theodosius Dobzhansky published Genetics and the Origin of Species in 1937 where he formulated the genetic framework for how speciation could occur.[1]

Other scientists noted the existence of allopatrically distributed pairs of species in nature such as Joel Asaph Allen (who coined the term "Jordan's Law", whereby closely related, geographically isolated species are often found divided by a physical barrier[1]) and Robert Greenleaf Leavitt[122]; however, it is thought that Wagner, Karl Jordan, and David Starr Jordan played a large role in the formation of allopatric speciation as an evolutionary concept;[123] where Mayr and Dobzhansky contributed to the formation of the modern evolutionary synthesis.

The late 20th century saw the development of mathematical models of allopatric speciation, leading to the clear theoretical plausibility that geographic isolation can result in the reproductive isolation of two populations of incipient species.[1]

Since the 1940s, allopatric speciation has been accepted.[124] Today, it is widely regarded as the most common form of speciation taking place in nature.[1] However, this is not without controversy, as both parapatric and sympatric speciation are both considered tenable modes of speciation that occur in nature.[124] Some researchers even consider there to be a bias in reporting of positive allopatric speciation events, and in one study reviewing 73 speciation papers published in 2009, only 30 percent that suggested allopatric speciation as the primary explanation for the patterns observed considered other modes of speciation as possible.[12]

Contemporary research relies largely on multiple lines of evidence to determine the mode of a speciation event; that is, determining patterns of geographic distribution in conjunction with phylogenetic relatedness based on molecular techniques.[1] This method was effectively introduced by John D. Lynch in 1986 and numerous researchers have employed it and similar methods, yielding enlightening results.[125] Correlation of geographic distribution with phylogenetic data also spawned a sub-field of biogeography called vicariance biogeography[1] developed by Joel Cracraft, James Brown, Mark V. Lomolino, among other biologists specializing in ecology and biogeography. Similarly, full analytical approaches have been proposed and applied to determine which speciation mode a species underwent in the past using various approaches or combinations thereof: species-level phylogenies, range overlaps, symmetry in range sizes between sister species pairs, and species movements within geographic ranges.[35] Molecular clock dating methods are also often employed to accurately gauge divergence times that reflect the fossil or geological record[1] (such as with the snapping shrimp separated by the closure of the Isthmus of Panama[51] or speciation events within the genus Cyclamen[126]). Other techniques used today have employed measures of gene flow between populations,[12] ecological niche modelling (such as in the case of the Myrtle and Audubon's warblers[127] or the environmentally-mediated speciation taking place among dendrobatid frogs in Ecuador[125]), and statistical testing of monophyletic groups.[128] Biotechnological advances have allowed for large scale, multi-locus genome comparisons (such as with the possible allopatric speciation event that occurred between ancestral humans and chimpanzees[129]), linking species' evolutionary history with ecology and clarifying phylogenetic patterns.[130]

References

  1. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 Jerry A. Coyne and H. Allen Orr (2004), Speciation, Sinauer Associates, pp. 83–124, ISBN 0-87893-091-4
  2. 1 2 3 4 5 Richard G. Harrison (2012), "The Language of Speciation", Evolution, 66 (12): 3643–3657, doi:10.1111/j.1558-5646.2012.01785.x
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Further reading

Mathematical models of reproductive isolation

  • H. Allen Orr and Michael Turelli (2001), "The evolution of postzygotic isolation: Accumulating Dobzhansky-Muller incompatibilities", Evolution, 55 (6): 1085–1094 
  • H. Allen Orr and Lynne H. Orr (1996), "Waiting for Speciation: The Effect of Population Subdivision on the Time to Speciation", Evolution, 50 (5): 1742–1749 
  • H. Allen Orr (1995), "The Population Genetics of Speciation: The Evolution of Hybrid Incompatibilities", Genetics, 139: 1805–1813 
  • Masatoshi Nei, Takeo Maruyama, and Chung-i Wu (1983), "Models of Evolution of Reproductive Isolation", Genetics, 103: 557–579 
  • Masatoshi Nei (1976), "Mathematical Models of Speciation and Genetic Distance", Population genetics and ecology: 723–766 
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