Peripatric speciation

Comparison of four modes of speciation: allopatric, peripatric, parapatric and sympatric.

Peripatric speciation is a mode of speciation in which a new species is formed from an isolated peripheral population.[1] 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.[2] 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 (e.g. sister species); their distribution being the result of peripatric speciation. An alternative model of peripatric speciation, centrifugal speciation, posits that a species' population experiences periods of geographic range expansion followed by shrinking periods, leaving behind small isolated populations on the periphery of the main population. Other models have involved the effects of sexual selection on limited population sizes.

The existence of peripatric speciation is supported by laboratory experiments and empirical evidence.[1] Scientists observing the patterns of a species biogeographic distribution and its phylogenetic relationships are able to reconstruct the historical process by which they diverged. Further, oceanic islands are often the subject of peripatric speciation research due to their isolated habitats—with the Hawaiian Islands widely represented in much of the scientific literature.

History

Peripatric speciation was first proposed by Ernst Mayr in 1954[3] and fully theoretically modeled in 1982.[4] It is related to the founder effect, where small living populations may undergo selection bottlenecks.[5] The founder effect is based on models that suggest peripatric speciation can occur by the interaction of selection and genetic drift,[1] which may play a significant role.[6] In 1976 and 1980, the Kaneshiro model of peripatric speciation was developed by Kenneth Y. Kaneshiro which focused on sexual selection as a driver for speciation during population bottlenecks.[7][8][9]

Models

Peripatric

Peripatric speciation models are identical to models of vicariance (allopatric speciation).[1] Requiring both geographic separation and time, speciation can result as a predictable byproduct.[10] Peripatry can be distinguished from allopatric speciation by three key features:[1]

The size of a 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—sometimes rapid—speciation events.[1] Furthermore, two important predictions are invoked, namely that geological or climactic changes cause populations to become locally fragmented (or regionally when considering allopatric speciation), and that an isolated population's reproductive traits evolve enough as to prevent interbreeding upon potential secondary contact.[11]

The peripatric model results in, what have been called, progenitor-derivative species pairs, whereby the derivative species (the peripherally isolated population)—geographically and genetically isolated from the progenitor species—diverges.[12] A specific phylogenetic signature results from this mode of speciation. That is, the central population remains pleisomorphic, while the peripheral isolates become apomorphic.[13]

One possible consequence of peripatric speciation is that a geographically widespread ancestral species becomes paraphyletic, thereby becoming a paraspecies.[14] The concept of a paraspecies is therefore a logical consequence of the evolutionary species concept, by which one species gives rise to a daughter species.[15]

Figure 2a: Peripatric speciation
Figure 2b: Centrifugal speciation
Diagrams representing the process of peripatric and centrifugal speciation. In peripatry, a small population becomes isolated on the periphery of the central population evolving reproductive isolation (blue) due to reduced gene flow. In centrifugal speciation, an original population (green) range expands and contracts, leaving an isolated fragment population behind. The central population (changed to blue) evolves reproductive isolation in contrast to peripatry.

Centrifugal speciation

William Louis Brown, Jr. proposed an alternative model of peripatric speciation in 1957 called centrifugal speciation. This model contrasts with peripatric speciation by virtue of the origin of the genetic novelty that leads to reproductive isolation.[16] A population of a species experiences periods of geographic range expansion followed by periods of contraction. During the contraction phase, fragments of the population become isolated as small refugial populations on the periphery of the central population (see figure 2b). Because of the large size and potentially greater genetic variation within the central population, mutations arise more readily. These mutations are left in the isolated peripheral populations, whereby, promoting reproductive isolation. Consequently, Brown suggested that during another expansion phase, the central population would overwhelm the peripheral populations, hindering speciation. However, if the species finds a specialized ecological niche, the two may coexist.[17][18] The phylogenetic signature of this model is that the central population becomes derived, while the peripheral isolates stay pleisomorphic[13]—the reverse of the general model.

Centrifugal speciation has been largely ignored in the scientific literature, often dominated by the traditional model of peripatric speciation.[19][16][13] Despite this, Brown cited a wealth of evidence to support his model, of which has not yet been refuted.[17]

Peromyscus polionotus and P. melanotis (the peripherally isolated species from the central population of P. maniculatus) arose via the centrifugal speciation model.[20] Centrifugal speciation may have taken place in tree kangaroos, South American frogs (Ceratophrys), shrews (Crocidura), and primates (Presbytis melalophos).[19] John C. Briggs associates centrifugal speciation with centers of origin, contending that the centrifugal model is better supported by the data, citing species patterns from the proposed 'center of origin' within the Indo-West Pacific[19]

Kaneshiro model

When a sexual species experiences a population bottleneck—that is, when the genetic variation is reduced due to small population size—mating discrimination among females may be altered by the decrease in courtship behaviors of males.[9] Sexual selection pressures may become weakened by this in an isolated peripheral population, and as a by-product of the altered mating recognition system, secondary sexual traits may appear.[7] Eventually, a growth in population size paired with novel female mate preferences will give rise to reproductive isolation from the main population-thereby completing the peripatric speciation process.[8]

Support for this model comes from experiments and observation of species that exhibit asymmetric mating patterns such as the Hawaiian Drosophila species[21][22] or the Hawaiian cricket Laupala.[23] However, this model has not been entirely supported by experiments, and therefore, it may not represent a plausible process of peripatric speciation that takes place in nature.[9]

Evidence

Species patterns on islands and archipelagos

Island species provide direct evidence of speciation occurring peripatrically in such that, "the presence of endemic species on oceanic islands whose closest relatives inhabit a nearby continent" must have originated by a colonization event.[1] Comparative phylogeography of oceanic archipelagos shows consistent patterns of sequential colonization and speciation along island chains, most notably on the Azores islands, Canary Islands, Society Islands, Marquesas Islands, Galápagos Islands, Austral Islands, and the Hawaiian Islands—all of which express geological patterns of spatial isolation and, in some cases, linear arrangement.[24]

Hawaiian archipelago

Figure 3a: Colonization events of species from the genus Cyanea (green) and species from the genus Drosophila (blue) on the Hawaiian island chain. Islands age from left to right, (Kauai being the oldest and Hawaii being the youngest). Speciation arises peripatrically as they spatiotemporally colonize new islands along the chain. Lighter blue and green indicate colonization in the reverse direction from young-to-old.
Figure 3b: A map of the Hawaiian archipelago showing the colonization routes of Theridion grallator superimposed. Purple lines indicate colonization occurring in conjunction with island age where light purple indicates backwards colonization. T. grallator is not present on Kauai or Niihau so colonization may have occurred from there, or the nearest continent.

Drosophila species on the Hawaiian archipelago have helped researchers understand speciation processes in great detail. It is well established that Drosophila has undergone an adaptive radiation into hundreds of endemic species on the Hawaiian island chain;[1][25] originating from a single common ancestor (supported from molecular analysis).[26] Studies consistently find that colonization of each island occurred from older to younger islands, and in Drosophila, speciating peripatrically at least fifty percent of the time.[1] In conjunction with Drosophila, Hawaiian lobeliads (Cyanea) have also undergone an adaptive radiation, with upwards of twenty-seven percent of extant species arising after new island colonization—exemplifying peripatric speciation—once again, occurring in the old-to-young island direction.[27][28][29] (See figure 3a).

Other endemic species in Hawaii also provide evidence of peripatric speciation such as the endemic flightless crickets (Laupala). It has been estimated that, "17 species out of 36 well-studied cases of [Laupala] speciation were peripatric".[1][30] Plant species in genera's such as Dubautia, Wilkesia, and Argyroxiphium have also radiated along the archipelago.[31]

Tetragnatha spiders have also speciated peripatrically on the Hawaiian islands,[32][33][1] Numerous arthropods have been documented existing in patterns consistent with the geologic evolution of the island chain, in such that, phylogenetic reconstructions find younger species inhabiting the geologically younger islands and older species inhabiting the older islands (or in some cases, ancestors date back to when islands currently below sea level were exposed). Spiders such as those from the genus Orsonwelles exhibit patterns compatible with the old-to-young geology.[34] Other endemic genera such as Argyrodes have been shown to have speciated along the island chain.[35] Pagiopalus, Pedinopistha, and part of the Thomisidae family have adaptively radiated along the island chain,[36] as well as the Lycosidae family of wolf spiders.[37]

A host of other Hawaiian endemic arthropod species and genera have had their speciation and phylogeographical patterns studied: the Drosophila grimshawi species complex,[38] damselflies (Megalagrion xanthomelas and Megalagrion pacificum),[39] Doryonychus raptor, Littorophiloscia hawaiiensis, Anax strenuus, Nesogonia blackburni, Theridion grallator[40] (see figure 3b), Vanessa tameamea, Hyalopeplus pellucidus, Coleotichus blackburniae, Labula, Hawaiioscia, Banza (in the Tettigoniidae family), Caconemobius, Eupethicea, Ptycta, Megalagrion, Prognathogryllus, Nesosydne, Cephalops, Trupanea, and the tribe Platynini—all suggesting repeated radiations among the islands.[41]

Other animals besides insects show this same pattern such as the Hawaiian amber snail (Succinea caduca),[42] and ‘Elepaio flycatchers.[43]

Other islands

Phylogenetic studies of a species of crab spider (Misumenops rapaensis) in the genus Thomisidae located on the Austral Islands have established the, "sequential colonization of [the] lineage down the Austral archipelago toward younger islands". Interestingly, M. rapaensis has been traditionally thought of as a single species; whereas this particular study found distinct genetic differences corresponding to the sequential age of the islands.[44]

Species patterns on continents

Figure 3c: Satellite image of the Noel Kempff Mercado National Park in Bolivia (outlined in green). The white arrow indicates the location of the isolated forest fragment.

The occurrence of peripatry on continents is more difficult to detect due to the possibility of vicariant explanations being equally likely.[1] However, studies concerning the Californian plant species Clarkia biloba and C. biloba strongly suggest a peripatric origin.[45] In addition, a great deal of research has been conducted on several species of land snails involving chirality that suggests peripatry (with some authors noting other possible interpretations).[1]

The chestnut-tailed antbird is located within the Serrania de Huanchaca in Bolivia. Within this region exists an fringe patch of forest (see figure 3c) estimated to have been isolated for 1000–3000 years. The population of antbirds that reside in the isolated patch express significant song divergence; thought to be an "early step" in the process of peripatric speciation. Further, peripheral isolation "may partly explain the dramatic diversification of suboscines in Amazonia".[11]

A study by Lucinda P. Lawson et al. found evidence for the occurrence of peripatric speciation in the montane spiny throated reed frog species complex (genus: Hyperolius). Lawson maintains that the species' geographic ranges within the Eastern Afromontane Biodiversity Hotspot support a peripatric model that is driving speciation; suggesting that this mode of speciation may play a significant role in "highly fragmented ecosystems".[2]

In a study of the phylogeny and biogeography of the land snail genus Monacha, the species M. ciscaucasica is thought to have speciated peripatrically from a population of M. roseni. In addition, M. claussi consists of a small population located on the peripheral of the much larger range of M. subcarthusiana suggesting that it also arose by peripatric speciation.[46]

Red spruce (Picea rubens) has arisen from an isolated population of black spruce (Picea mariana). During the Pleistocene, a population of black spruce became geographically isolated, likely due to glaciation. The geographic range of the black spruce is much larger than the red spruce. The red spruce has significantly lower genetic diversity in both its DNA and its mitochondrial DNA than the black spruce.[47][48] Furthermore, the genetic variation of the red spruce has no unique mitochondrial haplotypes, only subsets of those in the black spruce; suggesting that the red spruce speciated peripatrically from the black spruce population.[49][50][51] It is thought that the entire Picea genus in North America has been diversified by the process of peripatric speciation, as numerous pairs of closely related species in the genus have smaller southern population ranges; and those with overlapping ranges often exhibit weak reproductive isolation.[52][48]

Using a phylogeographic approach paired with ecological niche models (i.e. prediction and identification of expansion and contraction species ranges into suitable habitats based on current ecological niches, correlated with fossil and molecular data), researchers found that the prairie dog species Cynomys mexicanus speciated peripatrically from Cynomys ludovicianus approximately 230,000 years ago. North American glacial cycles promoted range expansion and contraction of the prairie dogs, leading to the isolation of a relic population in a refugium located in the present day Coahuila, Mexico.[53] This distribution and paleobiogeographic pattern correlates with other species expressing similar biographic range patterns[53] such as with the Sorex cinereus complex.[54]

Laboratory experiments

Peripatric speciation has been researched in both laboratory studies and nature. Coyne and Orr in Speciation suggest that most laboratory studies of allopatric speciation are also examples of peripatric speciation due to their small population sizes and the inevitable divergent selection that they undergo.[1]

Much of the laboratory research concerning peripatry is inextricably linked to founder effect research. Coyne and Orr conclude that selection's role in speciation is well established, whereas genetic drift's role is unsupported by experimental and field data—suggesting that founder-effect speciation does not occur.[55] Nevertheless, a great deal of research has been conducted on the matter, and one study conducted involving bottleneck populations of Drosophila pseudoobscura found evidence of isolation after a single bottleneck.[56][57]

Below is a non-exhaustive table of laboratory experiments focused explicitly on peripatric speciation. Most of the studies also conducted experiments on vicariant speciation as well. The "replicates" column signifies the number of lines used in the experiment—that is, how many independent populations were used (not the population size or the number of generations performed).[9]

Species Replicates Reference Year
Drosophila adiastola 1 [58] 1979
Drosophila silvestris 1 [59] 1980
Drosophila pseudoobscura 8 [60] 1985
Drosophila simulans 8 [61] 1985
Musca domestica 6 [62] 1991
Drosophila pseudoobscura 42 [63] 1993
Drosophila melanogaster 50 [64] 1998
Drosophila melanogaster 19; 19 [65] 1999
Drosophila grimshawi 1 [9] N/A

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  65. ↑ Mooers, A. Ø., Rundle, H. D. and Whitlock, M. C. (1999), "The effects of selection and bottlenecks on male mating success in peripheral isolates", American Naturalist, 153: 437–444
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