Parapatric speciation

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A diagram representing population subject to a selective gradient of phenotypic or genotypic frequencies (a cline). Each end of the gradient experiences different selective conditions (divergent selection). Reproductive isolation occurs upon the formation of a hybrid zone. In most cases, the hybrid zone is eliminated due to a selective disadvantage. This effectively completes the speciation process. Parapatric Speciation Schematic.svg
A diagram representing population subject to a selective gradient of phenotypic or genotypic frequencies (a cline). Each end of the gradient experiences different selective conditions (divergent selection). Reproductive isolation occurs upon the formation of a hybrid zone. In most cases, the hybrid zone is eliminated due to a selective disadvantage. This effectively completes the speciation process.

In parapatric speciation, two subpopulations of a species evolve reproductive isolation from one another while continuing to exchange genes. This mode of speciation has three distinguishing characteristics: 1) mating occurs non-randomly, 2) gene flow occurs unequally, and 3) populations exist in either continuous or discontinuous geographic ranges. This distribution pattern may be the result of unequal dispersal, incomplete geographical barriers, or divergent expressions of behavior, among other things. Parapatric speciation predicts that hybrid zones will often exist at the junction between the two populations.

Contents

In biogeography, the terms parapatric and parapatry are often used 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. Parapatry is a geographical distribution opposed to sympatry (same area) and allopatry or peripatry (two similar cases of distinct areas).

Various "forms" of parapatry have been proposed and are discussed below. Coyne and Orr in Speciation categorise these forms into three groups: clinal (environmental gradients), "stepping-stone" (discrete populations), and stasipatric speciation in concordance with most of the parapatric speciation literature. [1] : 111  Henceforth, the models are subdivided following a similar format.

Charles Darwin was the first to propose this mode of speciation. It was not until 1930, when Ronald Fisher published The Genetical Theory of Natural Selection where he outlined a verbal theoretical model of clinal speciation. In 1981, Joseph Felsenstein proposed an alternative, "discrete population" model (the "stepping-stone model). Since Darwin, a great deal of research has been conducted on parapatric speciation—concluding that its mechanisms are theoretically plausible, "and has most certainly occurred in nature". [1] : 124 

Models

Mathematical models, laboratory studies, and observational evidence supports the existence of parapatric speciation's occurrence in nature. The qualities of parapatry imply a partial extrinsic barrier during divergence; [2] thus leading to a difficulty in determining whether this mode of speciation actually occurred, or if an alternative mode (notably, allopatric speciation) can explain the data. This problem poses the unanswered question as to its overall frequency in nature. [1] : 124 

Parapatric speciation can be understood as a level of gene flow between populations where in allopatry (and peripatry), in sympatry, and midway between the two in parapatry. [3] Intrinsic to this, parapatry covers the entire continuum; represented as . Some biologists reject this delineation, advocating the disuse of the term "parapatric" outright, "because many different spatial distributions can result in intermediate levels of gene flow". [4] Others champion this position and suggest the abandonment of geographic classification schemes (geographic modes of speciation) altogether. [5]

Natural selection has been shown to be the primary driver in parapatric speciation (among other modes), [6] and the strength of selection during divergence is often an important factor. [7] Parapatric speciation may also result from reproductive isolation caused by social selection: individuals interacting altruistically. [8]

Environmental gradients

Due to the continuous nature of a parapatric population distribution, population niches will often overlap, producing a continuum in the species' ecological role across an environmental gradient. [9] Whereas in allopatric or peripatric speciation—in which geographically isolated populations may evolve reproductive isolation without gene flow—the reduced gene flow of parapatric speciation will often produce a cline in which a variation in evolutionary pressures causes a change to occur in allele frequencies within the gene pool between populations. This environmental gradient ultimately results in genetically distinct sister species.

Fisher's original conception of clinal speciation relied on (unlike most modern speciation research) the morphological species concept. [1] : 113  With this interpretation, his verbal, theoretical model can effectively produce a new species; of which was subsequently confirmed mathematically. [10] [1] : 113  Further mathematical models have been developed to demonstrate the possibility of clinal speciation with most relying on, what Coyne and Orr assert are, "assumptions that are either restrictive or biologically unrealistic". [1] : 113 

A mathematical model for clinal speciation was developed by Caisse and Antonovics that found evidence that, "both genetic divergence and reproductive isolation may therefore occur between populations connected by gene flow". [11] This research supports clinal isolation comparable to a ring species (discussed below), except that the terminal geographic ends do not meet to form a ring.

Doebeli and Dieckmann developed a mathematical model that suggested that ecological contact is an important factor in parapatric speciation and that, despite gene flow acting as a barrier to divergence in the local population, disruptive selection drives assortative mating; eventually leading to a complete reduction in gene flow. This model resembles reinforcement with the exception that there is never a secondary contact event. The authors conclude that, "spatially localized interactions along environmental gradients can facilitate speciation through frequency-dependent selection and result in patterns of geographical segregation between the emerging species." [9] However, one study by Polechová and Barton disputes these conclusions. [12]

Ring species

In a ring species, individuals are able to successfully reproduce (exchange genes) with members of their own species in adjacent populations occupying a suitable habitat around a geographic barrier. Individuals at the ends of the cline are unable to reproduce when they come into contact. Ring Species (gene flow around a barrier).png
In a ring species, individuals are able to successfully reproduce (exchange genes) with members of their own species in adjacent populations occupying a suitable habitat around a geographic barrier. Individuals at the ends of the cline are unable to reproduce when they come into contact.

The concept of a ring species is associated with allopatric speciation as a special case; [13] however, Coyne and Orr argue that Mayr's original conception of a ring species does not describe allopatric speciation, "but speciation occurring through the attenuation of gene flow with distance". They contend that ring species provide evidence of parapatric speciation in a non-conventional sense. [1] : 102–103  They go on to conclude that:

Nevertheless, ring species are more convincing than cases of clinal isolation for showing that gene flow hampers the evolution of reproductive isolation. In clinal isolation, one can argue that reproductive isolation was caused by environmental differences that increase with distance between populations. One cannot make a similar argument for ring species because the most reproductively isolated populations occur in the same habitat. [1] : 102 

Discrete populations

Referred to as a "stepping-stone" model by Coyne and Orr, it differs by virtue of the species population distribution pattern. Populations in discrete groups undoubtedly speciate more easily than those in a cline due to more limited gene flow. [1] : 115  This allows for a population to evolve reproductive isolation as either selection or drift overpower gene flow between the populations. The smaller the discrete population, the species will likely undergo a higher rate of parapatric speciation. [14]

Several mathematical models have been developed to test whether this form of parapatric speciation can occur, providing theoretical possibility and supporting biological plausibility (dependent on the models parameters and their concordance with nature). [1] : 115  Joseph Felsenstein was the first to develop a working model. [1] : 115  Later, Sergey Gavrilets and colleagues developed numerous analytical and dynamical models of parapatric speciation that have contributed significantly to the quantitative study of speciation. (See the "Further reading" section)

Para-allopatric speciation

Further concepts developed by Barton and Hewitt in studying 170 hybrid zones, suggested that parapatric speciation can result from the same components that cause allopatric speciation. Called para-allopatric speciation, populations begin diverging parapatrically, fully speciating only after allopatry. [15]

Stasipatric models

One variation of parapatric speciation involves species chromosomal differences. Michael J. D. White developed the stasipatric speciation model when studying Australian morabine grasshoppers ( Vandiemenella ). The chromosomal structure of sub-populations of a widespread species become underdominate; leading to fixation. Subsequently, the sub-populations expand within the species larger range, hybridizing (with sterility of the offspring) in narrow hybrid zones. [16] Futuyama and Mayer contend that this form of parapatric speciation is untenable and that chromosomal rearrangements are unlikely to cause speciation. [17] Nevertheless, data does support that chromosomal rearrangements can possibly lead to reproductive isolation, but it does not mean speciation results as a consequence. [1] : 259 

Evidence

Laboratory evidence

Very few laboratory studies have been conducted that explicitly test for parapatric speciation. However, research concerning sympatric speciation often lends support to the occurrence of parapatry. This is due to the fact that, in symaptric speciation, gene flow within a population is unrestricted; whereas in parapatric speciation, gene flow is limited—thus allowing reproductive isolation to evolve easier. [1] : 117  Ödeen and Florin complied 63 laboratory experiments conducted between the years 1950–2000 (many of which were discussed by Rice and Hostert previously [18] ) concerning sympatric and parapatric speciation. They contend that the laboratory evidence is more robust than often suggested, citing laboratory populations sizes as the primary shortcoming. [19]

Observational evidence

Parapatric speciation is very difficult to observe in nature. This is due to one primary factor: patterns of parapatry can easily be explained by an alternate mode of speciation. Particularly, documenting closely related species sharing common boundaries does not imply that parapatric speciation was the mode that created this geographic distribution pattern. [1] : 118  Coyne and Orr assert that the most convincing evidence of parapatric speciation comes in two forms. This is described by the following criteria:

Anthoxanthum odoratum AnthoxanthumOdoratum.jpg
Anthoxanthum odoratum

This has been exemplified by the grass species Agrostis tenuis that grows on soil contaminated with high levels of copper, leached from an unused mine. Adjacent is the non-contaminated soil. The populations are evolving reproductive isolation due to differences in flowering. The same phenomenon has been found in Anthoxanthum odoratum in lead and zinc contaminated soils. [20] [21] Speciation may be caused by allochrony. [22]

Clines are often cited as evidence of parapatric speciation and numerous examples have been documented to exist in nature; many of which contain hybrid zones. These clinal patterns, however, can also often be explained by allopatric speciation followed by a period of secondary contact—causing difficulty for researchers attempting to determine their origin. [1] : 118  [23] Thomas B. Smith and colleagues posit that large ecotones are "centers for speciation" (implying parapatric speciation) and are involved in the production of biodiversity in tropical rainforests. They cite patterns of morphologic and genetic divergence of the passerine species Andropadus virens . [24] Jiggins and Mallet surveyed a range of literature documenting every phase of parapatric speciation in nature positing that it is both possible and likely (in the studied species discussed). [25]

A study of tropical cave snails ( Georissa saulae ) found that cave-dwelling population descended from the above-ground population, likely speciating in parapatry. [26]

Partula snails on the island of Mo'orea have parapatrically speciated in situ after a single or a few colonization events, with some species expressing patterns of ring species. [27]

In the Tennessee cave salamander, timing of migration was used to infer the differences in gene flow between cave-dwelling and surface-dwelling continuous populations. Concentrated gene flow and mean migration time results inferred a heterogenetic distribution and continuous parapatric speciation between populations. [28]

Researchers studying Ephedra , a genus of gymnosperms in North American, found evidence of parapatric niche divergence for the sister species pairs E. californica and E. trifurca. [29]

One study of Caucasian rock lizards suggested that habitat differences may be more important in the development of reproductive isolation than isolation time. Darevskia rudis, D. valentini and D. portschinskii all hybridize with each other in their hybrid zone; however, hybridization is stronger between D. portschinskii and D. rudis, which separated earlier but live in similar habitats than between D. valentini and two other species, which separated later but live in climatically different habitats. [30]

Marine organisms

It is widely thought that parapatric speciation is far more common in oceanic species due to the low probability of the presence of full geographic barriers (required in allopatry). [31] Numerous studies conducted have documented parapatric speciation in marine organisms. Bernd Kramer and colleagues found evidence of parapatric speciation in Mormyrid fish ( Pollimyrus castelnaui ); [32] whereas Rocha and Bowen contend that parapatric speciation is the primary mode among coral-reef fish. [33] Evidence for a clinal model of parapatric speciation was found to occur in Salpidae. [31] Nancy Knowlton found numerous examples of parapatry in a large survey of marine organisms. [34]

See also

Related Research Articles

Speciation is the evolutionary process by which populations evolve to become distinct species. The biologist Orator F. Cook coined the term in 1906 for cladogenesis, the splitting of lineages, as opposed to anagenesis, phyletic evolution within lineages. Charles Darwin was the first to describe the role of natural selection in speciation in his 1859 book On the Origin of Species. He also identified sexual selection as a likely mechanism, but found it problematic.

Allopatric speciation – also referred to as geographic speciation, vicariant speciation, or its earlier name the dumbbell model – is a mode of speciation that occurs when biological populations become geographically isolated from each other to an extent that prevents or interferes with gene flow.

<span class="mw-page-title-main">Sympatric speciation</span> Evolution of a new species from an ancestor in the same location

In evolutionary biology, sympatric speciation is the evolution of a new species from a surviving ancestral species while both continue to inhabit the same geographic region. In evolutionary biology and biogeography, sympatric and sympatry are terms referring to organisms whose ranges overlap so that they occur together at least in some places. If these organisms are closely related, such a distribution may be the result of sympatric speciation. Etymologically, sympatry is derived from Greek συν (sun-) 'together', and πατρίς (patrís) 'fatherland'. The term was coined by Edward Bagnall Poulton in 1904, who explains the derivation.

<span class="mw-page-title-main">Haldane's rule</span> Observation in evolutionary biology

Haldane's rule is an observation about the early stage of speciation, formulated in 1922 by the British evolutionary biologist J. B. S. Haldane, that states that if — in a species hybrid — only one sex is inviable or sterile, that sex is more likely to be the heterogametic sex. The heterogametic sex is the one with two different sex chromosomes; in therian mammals, for example, this is the male.

<span class="mw-page-title-main">Peripatric speciation</span> Speciation in which a new species is formed from an isolated smaller peripheral population

Peripatric speciation is a mode of speciation in which a new species is formed from an isolated peripheral population. Since peripatric speciation resembles allopatric speciation, in that populations are isolated and prevented from exchanging genes, it can often be difficult to distinguish between them. Nevertheless, the primary characteristic of peripatric speciation proposes that one of the populations is much smaller than the other. The terms peripatric and peripatry are often used in biogeography, referring to organisms whose ranges are closely adjacent but do not overlap, being separated where these organisms do not occur—for example on an oceanic island compared to the mainland. Such organisms are usually closely related ; their distribution being the result of peripatric speciation.

<span class="mw-page-title-main">Sympatry</span> Biological concept

In biology, two related species or populations are considered sympatric when they exist in the same geographic area and thus frequently encounter one another. An initially interbreeding population that splits into two or more distinct species sharing a common range exemplifies sympatric speciation. Such speciation may be a product of reproductive isolation – which prevents hybrid offspring from being viable or able to reproduce, thereby reducing gene flow – that results in genetic divergence. Sympatric speciation may, but need not, arise through secondary contact, which refers to speciation or divergence in allopatry followed by range expansions leading to an area of sympatry. Sympatric species or taxa in secondary contact may or may not interbreed.

<span class="mw-page-title-main">Hybrid zone</span>

A hybrid zone exists where the ranges of two interbreeding species or diverged intraspecific lineages meet and cross-fertilize. Hybrid zones can form in situ due to the evolution of a new lineage but generally they result from secondary contact of the parental forms after a period of geographic isolation, which allowed their differentiation. Hybrid zones are useful in studying the genetics of speciation as they can provide natural examples of differentiation and (sometimes) gene flow between populations that are at some point between representing a single species and representing multiple species in reproductive isolation.

Genetic divergence is the process in which two or more populations of an ancestral species accumulate independent genetic changes (mutations) through time, often leading to reproductive isolation and continued mutation even after the populations have become reproductively isolated for some period of time, as there is not any genetic exchange anymore. In some cases, subpopulations cover living in ecologically distinct peripheral environments can exhibit genetic divergence from the remainder of a population, especially where the range of a population is very large. The genetic differences among divergent populations can involve silent mutations or give rise to significant morphological and/or physiological changes. Genetic divergence will always accompany reproductive isolation, either due to novel adaptations via selection and/or due to genetic drift, and is the principal mechanism underlying speciation.

The mechanisms of reproductive isolation are a collection of evolutionary mechanisms, behaviors and physiological processes critical for speciation. They prevent members of different species from producing offspring, or ensure that any offspring are sterile. These barriers maintain the integrity of a species by reducing gene flow between related species.

In biology, a cline is a measurable gradient in a single characteristic of a species across its geographical range. Clines usually have a genetic, or phenotypic character. They can show either smooth, continuous gradation in a character, or more abrupt changes in the trait from one geographic region to the next.

H. Allen Orr is the Shirley Cox Kearns Professor of Biology at the University of Rochester.

<span class="mw-page-title-main">Bateson–Dobzhansky–Muller model</span> Model of the evolution of genetic incompatibility

The Bateson–Dobzhansky–Muller model, also known as Dobzhansky–Muller model, is a model of the evolution of genetic incompatibility, important in understanding the evolution of reproductive isolation during speciation and the role of natural selection in bringing it about. The theory was first described by William Bateson in 1909, then independently described by Theodosius Dobzhansky in 1934, and later elaborated in different forms by Herman Muller, H. Allen Orr and Sergey Gavrilets.

<span class="mw-page-title-main">Ecological speciation</span>

Ecological speciation is a form of speciation arising from reproductive isolation that occurs due to an ecological factor that reduces or eliminates gene flow between two populations of a species. Ecological factors can include changes in the environmental conditions in which a species experiences, such as behavioral changes involving predation, predator avoidance, pollinator attraction, and foraging; as well as changes in mate choice due to sexual selection or communication systems. Ecologically-driven reproductive isolation under divergent natural selection leads to the formation of new species. This has been documented in many cases in nature and has been a major focus of research on speciation for the past few decades.

<span class="mw-page-title-main">Reinforcement (speciation)</span> Process of increasing reproductive isolation

Reinforcement is a process of speciation where natural selection increases the reproductive isolation between two populations of species. This occurs as a result of selection acting against the production of hybrid individuals of low fitness. The idea was originally developed by Alfred Russel Wallace and is sometimes referred to as the Wallace effect. The modern concept of reinforcement originates from Theodosius Dobzhansky. He envisioned a species separated allopatrically, where during secondary contact the two populations mate, producing hybrids with lower fitness. Natural selection results from the hybrid's inability to produce viable offspring; thus members of one species who do not mate with members of the other have greater reproductive success. This favors the evolution of greater prezygotic isolation. Reinforcement is one of the few cases in which selection can favor an increase in prezygotic isolation, influencing the process of speciation directly. This aspect has been particularly appealing among evolutionary biologists.

<span class="mw-page-title-main">History of speciation</span>

The scientific study of speciation — how species evolve to become new species — began around the time of Charles Darwin in the middle of the 19th century. Many naturalists at the time recognized the relationship between biogeography and the evolution of species. The 20th century saw the growth of the field of speciation, with major contributors such as Ernst Mayr researching and documenting species' geographic patterns and relationships. The field grew in prominence with the modern evolutionary synthesis in the early part of that century. Since then, research on speciation has expanded immensely.

<span class="mw-page-title-main">Evidence for speciation by reinforcement</span> Overview article

Reinforcement is a process within speciation where natural selection increases the reproductive isolation between two populations of species by reducing the production of hybrids. Evidence for speciation by reinforcement has been gathered since the 1990s, and along with data from comparative studies and laboratory experiments, has overcome many of the objections to the theory. Differences in behavior or biology that inhibit formation of hybrid zygotes are termed prezygotic isolation. Reinforcement can be shown to be occurring by measuring the strength of prezygotic isolation in a sympatric population in comparison to an allopatric population of the same species. Comparative studies of this allow for determining large-scale patterns in nature across various taxa. Mating patterns in hybrid zones can also be used to detect reinforcement. Reproductive character displacement is seen as a result of reinforcement, so many of the cases in nature express this pattern in sympatry. Reinforcement's prevalence is unknown, but the patterns of reproductive character displacement are found across numerous taxa, and is considered to be a common occurrence in nature. Studies of reinforcement in nature often prove difficult, as alternative explanations for the detected patterns can be asserted. Nevertheless, empirical evidence exists for reinforcement occurring across various taxa and its role in precipitating speciation is conclusive.

<span class="mw-page-title-main">Laboratory experiments of speciation</span> Biological experiments

Laboratory experiments of speciation have been conducted for all four modes of speciation: allopatric, peripatric, parapatric, and sympatric; and various other processes involving speciation: hybridization, reinforcement, founder effects, among others. Most of the experiments have been done on flies, in particular Drosophila fruit flies. However, more recent studies have tested yeasts, fungi, and even viruses.

This glossary of genetics and evolutionary biology is a list of definitions of terms and concepts used in the study of genetics and evolutionary biology, as well as sub-disciplines and related fields, with an emphasis on classical genetics, quantitative genetics, population biology, phylogenetics, speciation, and systematics. Overlapping and related terms can be found in Glossary of cellular and molecular biology, Glossary of ecology, and Glossary of biology.

Allochronic speciation is a form of speciation arising from reproductive isolation that occurs due to a change in breeding time that reduces or eliminates gene flow between two populations of a species. The term allochrony is used to describe the general ecological phenomenon of the differences in phenology that arise between two or more species—speciation caused by allochrony is effectively allochronic speciation.

In biology, parallel speciation is a type of speciation where there is repeated evolution of reproductively isolating traits via the same mechanisms occurring between separate yet closely related species inhabiting different environments. This leads to a circumstance where independently evolved lineages have developed reproductive isolation from their ancestral lineage, but not from other independent lineages that inhabit similar environments. In order for parallel speciation to be confirmed, there is a set of three requirements that has been established that must be met: there must be phylogenetic independence between the separate populations inhabiting similar environments to ensure that the traits responsible for reproductive isolation evolved separately, there must be reproductive isolation not only between the ancestral population and the descendent population, but also between descendent populations that inhabit dissimilar environments, and descendent populations that inhabit similar environments must not be reproductively isolated from one another. To determine if natural selection specifically is the cause of parallel speciation, a fourth requirement has been established that includes identifying and testing an adaptive mechanism, which eliminates the possibility of a genetic factor such as polyploidy being the responsible agent.

References

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  28. ↑ M. L. Niemiller, B. M. Fitzpatrick, and B. T. Miller (2008), "Recent divergence with gene flow in Tennessee cave salamanders (Plethodontidae: Gyrinophilus) inferred from gene genealogies", Molecular Ecology, 17 (9): 2258–2275, Bibcode:2008MolEc..17.2258N, doi: 10.1111/j.1365-294X.2008.03750.x , PMID   18410292, S2CID   20761880 {{citation}}: CS1 maint: multiple names: authors list (link)
  29. ↑ I. Loera, V. Sosa, and S. M. Ickert-Bond (2012), "Diversification in North American arid lands: niche conservatism, divergence and expansion of habitat explain speciation in the genus Ephedra", Molecular Phylogenetics and Evolution, 65 (2): 437–450, doi:10.1016/j.ympev.2012.06.025, PMID   22776548 {{citation}}: CS1 maint: multiple names: authors list (link)
  30. ↑ David Tarkhnishvili, Marine Murtskhvaladze, and Alexander Gavashelishvili (2013), "Speciation in Caucasian lizards: climatic dissimilarity of the habitats is more important than isolation time", Biological Journal of the Linnean Society, 109 (4): 876–892, doi: 10.1111/bij.12092 {{citation}}: CS1 maint: multiple names: authors list (link)
  31. 1 2 John C. Briggs (1999), "Modes of Speciation: Marine Indo-West Pacific", Bulletin of Marine Science, 65 (3): 645–656
  32. ↑ Bernd Kramer; et al. (2003), "Evidence for parapatric speciation in the Mormyrid fish, Pollimyrus castelnaui (Boulenger, 1911), from the Okavango–Upper Zambezi River Systems: P. marianne sp. nov., defined by electric organ discharges, morphology and genetics" (PDF), Environmental Biology of Fishes, 67 (1): 47–70, Bibcode:2003EnvBF..67...47K, doi:10.1023/A:1024448918070, S2CID   25826083
  33. ↑ L. A. Rocha and B. W. Bowen (2008), "Speciation in coral-reef fishes", Journal of Fish Biology, 72 (5): 1101–1121, Bibcode:2008JFBio..72.1101R, doi:10.1111/j.1095-8649.2007.01770.x
  34. ↑ Nancy Knowlton (1993), "Sibling Species in the Sea", Annual Review of Ecology and Systematics, 24: 189–216, doi:10.1146/annurev.es.24.110193.001201

Further reading

Quantitative speciation research

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