What occurs when a few individuals from a larger population forms a new colony?

Evidence for and against Peripatric Speciation

Peripatric speciation was favored by many evolutionary biologists in the 1970s and 1980s. Widespread support for peripatric speciation was fostered in part by extensive research on Hawaiian picture-winged Drosophila (Fig. 5), led by Hampton Carson, Kenneth Kaneshiro, and Allan Templeton (Carson and Kaneshiro, 1976; Carson, 1983; Carson and Templeton, 1984). High endemnicity of species to single islands, with more recently derived species tending to occur on geologically younger islands, provides clear evidence that most speciation events in this group are associated with the colonization of newly formed islands from parental populations on older islands. Additional biogeographical evidence from a wide variety of island taxa provides a obvious link between speciation and dispersal, such as for flightless crickets in the Hawaiian genus Laupala (Mendelson and Shaw, 2005) and Darwin׳s finches in the Galapagos (Vincek et al., 1997). The leaders of the Drosophila research program also developed their own genetic models of divergence. Although their models differed somewhat from Mayr’s, most emphasized the role of the founder effect and the importance of changes in the genetic environment within a peripheral isolate.

Evidence of peripatric speciation is harder to come by for continental organisms, possibly because of a greater likelihood that the biogeographical evidence will be lost as a consequence of postspeciation range expansions. However, by comparing the relative sizes of the geographic distributions of species to their times of divergence, Barraclough and Vogler (2000) showed that many recently split lineages from a wide variety of taxa show unexpectedly high asymmetry with respect to their geographic ranges. Although other explanations are possible, a large asymmetry in geographic range between parental and daughter species at the time of speciation is consistent with peripatric speciation.

Phylogeographic studies also provide support for peripatric speciation if a putative daughter species possesses a small subset of the genetic diversity found in the parental species, indicating that the daughter species was formed from a relatively small population (Ovenden and White, 1990); the parental species’ genome may also have many loci that are paraphyletic with respect to the daughter species, meaning that some alleles or haplotypes found in the parent are more closely related to those found in the daughter species, but all alleles or haplotypes in the daughter species are derived exclusively from a single lineage (Harrison, 1991; Marko, 1998). One of the most widely cited examples of peripatric speciation comes from a pair of species in the plant genus Clarkia, in which the putative daughter species is restricted to only two sites at the edge of the geographic range of the parental species in central California; the daughter species possesses less phenotypic variation and only a subset of the genetic diversity of the parental species (Gottlieb, 2004). This mode of speciation could be common in plants, in which relatively small genetic changes have the potential to rapidly reproductively isolate a localized population.

Even if many species arise as a consequence of colonization events (the existence of many endemic species on isolated islands and archipelagos makes this conclusion self-evident), the mechanism driving genetic divergence in a peripheral isolate cannot necessarily be attributed to the founder effect. In fact, as biogeographical evidence supporting peripatric speciation has grown, support for the role of the founder effect has diminished, mainly for two reasons. First, few species putatively formed in peripatry show strong genetic evidence of a severe bottleneck in their recent past (Barton and Charlesworth, 1984). Furthermore, even if a putative daughter species has low genetic variation across its entire geographic range, it remains difficult to determine if a bottleneck happened at the same time as speciation or after (Harrison, 1991). For example, low genetic variation throughout nearly all of the geographic of the marine snail N. emarginata (relative to it׳s sister-species) in California is consistent with peripatric speciation, except that the southermost population of this species has as much genetic variation as any population in the parental species, indicating that a severe bottleneck was not involved in speciation (Marko, 1998). Extinction of (or failure to sample) the high diversity population, would easily lead to the erroneous conclusion of a founder effect. In this case, low diversity across most of the daughter species’ range is likely a consequence of a postglacial population expansion that happened after a period of allopatry.

A second reason why the popularity of genetic models of peripatric speciation has waned is that theoretical population geneticists have developed persuasive arguments against the potential role of the founder effect (Barton and Charlesworth, 1984; Charlesworth, 1997). Although more recent models of founder effect speciation have been more successful demonstrating that bottlenecks may actually facilitate speciation (Gavrilets and Hastings, 1996), laboratory tests involving bottlenecked populations of fruit flies (Drosophila) provide equivocal results (Powell, 1978; Dodd and Powell, 1985). In fact, the mixture of outcomes from these experiments have been interpreted by both proponents and critics of peripatric speciation as either favoring or refuting, respectively, the importance of the founder effect in speciation.

Peripatric Speciation and the Founder Effect Principle

There are several examples in which species appear to have evolved in small, isolated populations at the periphery of the range of a sister species. Unlike the slow rate of evolution in dichopatric speciation, peripatric speciation is postulated to take a relatively short time. How and how often this divergence occurs is controversial (Barton, 1996; Hollocher, 1996).

Three models, each based on a founder event in which a population is established by only a few individuals, have been proposed to account for the rapid evolution of species observed on islands and elsewhere (Figure 1c). The founder effect principle was developed by Mayr (1954). It is based on the assumption that reproductive isolation from the parent species can evolve rapidly in a population established by a very small number of founding individuals (i.e., 2–10). He postulated that in such populations a genetic revolution could take place as a by-product of inbreeding, selection, drift, and genome reorganization. While the population is small, these genetic changes may promote substantial morphological and ecological shifts.

A modification of the founder effect principle was proposed by Carson (1975). In his founder-flush model of speciation, isolated populations undergo a series of population expansions and drastic contractions to a very small number of individuals. Carson believes that founder-flush speciation can occur only in certain cross fertilizing diploid organisms with “open” genetic systems. The genome in such organisms represents a clique of harmoniously collaborating or coadapted genes united by strong epistatic interactions. Their genomes also have abundant pleiotropic interacting genetic polymorphisms and share a high recombination index. Carson hypothesized that these attributes provide great genetic flexibility that predisposes such organisms to speciate by the founder-flush process.

In Carson's view, the drastic events required to reorganize the original genetic system and restore new balances that are incompatible with ancestors are accomplished during cycles of the founder-flush process. Selection, which is relaxed during the flush phase of population expansion, is greatly intensified as the population crashes. Repeated disorganization and reconstitution of the genome results in the rapid evolution of reproductive isolation.

Templeton (1980) proposed a third modification of founder-induced speciation that involves a genetic transilience (Carson and Templeton, 1984). It is similar to Carson's founder-flush speciation but requires changes in only one or a few segregating units, commonly with epistatic modifiers responsible for reproductive isolation that occurs when a population rapidly passes through an extremely unstable intermediate genetic state. As in the case of the founder-flush model, a genetic transilience involves strong inbreeding and large variance in population size. The critical trigger that initiates a transilience requires a reweighting of fitness components owing to drift-induced shifts in allele frequencies at one or more major loci that have pleiotropic effects on reproductive isolation.

It seems clear that speciation may occur rapidly following the geographic isolation of a small population. It is not clear, however, whether speciation results from a founder-flush or transilience process or solely from natural selection in response to factors such as runaway sexual selection or rapid adaptation to divergent ecological and reproductive conditions. Because conditions required for stochastic transitions are severe and well documented cases are lacking in which drastic genetic changes caused by founder effects result in speciation, it appears that the process of speciation in small, peripheral populations is the same as that which occurs in dichopatric speciation. Although certain kinds of epistasis can promote strong reproductive isolation, divergence occurs by selection and not random genetic drift (Barton, 1996).

Peripatric or Founder Effect Speciation

Peripatric speciation represents a variation on allopatric speciation. In this case, a small population forms at the periphery of a larger population. This type of geographical isolation can happen anywhere, but is most easy to visualize in the situation of founders colonizing oceanic islands or, more generally, isolated pockets of habitat. Because the founding of peripheral populations can sometimes involve the movement of only a few individuals (or even a single gravid female), this type of speciation has also become known as founder effect speciation. The emphasis here is on the interaction between genetic drift and natural or sexual selection that occurs during the early stages of speciation.

If a new population is founded by a small number of individuals, just by chance the genetic composition of the founding population may differ significantly from that of the original source population because of genetic drift (see Genetic Drift). The population need not remain small for very long in order for this sampling effect to influence the future evolutionary trajectory of the population. In addition to this immediate genetic change, oftentimes small populations founded in peripheral habitats or on islands also experience changed environments (both the physical environment, including such things as the quality of the habitat, the distribution of resources, or the presence of competitors or predators, as well as the mating environment, represented by a shift in the distribution of available mating types and preferences), creating new selection regimes. Even in the complete absence of new selective environments, the shift in allele frequencies alone can potentially have a profound effect on how the population will respond to selection because of the changed internal genetic environment that results from drift. The combination of shifting gene frequencies by drift and the presence of potentially new selection regimes under this scenario has led some researchers to propose that this type of speciation can occur more rapidly than the more standard form of allopatric speciation which generally involves populations of larger size and less drastic changes in the physical and mating environment on isolation (for reviews, see Hollocher article in Grant, 1998; Templeton, 2008).

The theoretical framework used to justify the conclusion that speciation would be accelerated during founder effect speciation stems directly from Wright's model of an adaptive landscape (see Natural Selection and Genetic Drift). A major underlying genetic assumption that enters into the idea that the random sampling of alleles during the founder event can have a profound effect on the evolutionary trajectory of a population is that epistasis (where interactions between alleles at different loci produce phenotypic effects that are not predicted by the action of the individual allelic effects considered alone) and pleiotropy (where a single locus can directly influence more than one phenotypic trait) are quite common. It is under the assumptions of this type of genetic architecture that fitness peaks of varying heights will exist in the adaptive landscape and where random shifts in allele frequencies can have profound effects (e.g., see Gavrilets and Hastings, 1996; Gavrilets, 2004). If allelic effects governing traits important in speciation are more additive (where interactions between alleles at different loci are minimal), then allele frequency changes will not necessarily impact the trajectory of natural selection greatly.

Much of the debate surrounding the likelihood of founder effects accelerating the process of speciation has focused on the specific influence drift alone would have on the probability of shifting from one fitness peak to another (for a reviews, see the Barton and Hollocher articles in Grant, 1998; Coyne and Orr, 2004; Gavrilets, 2004). What has emerged from these theoretical studies has been the idea that the actual size of the founding population does not play as crucial a role in determining the probability of shifting from one fitness peak to another as does the underlying genetic architecture of fitness. On the basis of these theoretical results, researchers have begun to shift their focus to evaluating the genetic architecture underlying traits that change during speciation to see how often epistasis is an important component (see Genetic Patterns and Processes of Species Differentiation; see also Phillips, 2008). In addition to the genetic architecture influencing rates of change, the actual nature of the trait itself can affect the type of response that is expected under founder effect speciation. Reproductive isolation (both prezygotic and postzygotic) can be particularly susceptible to rapid change under this scenario because of the tight coevolution of male and female traits that normally occurs via sexual selection (see Sexual Selection). The random sampling of individuals during a founder event can easily move the population away from the stable equilibrium that characterizes the reproductive system in the original population. Reestablishment of a new equilibrium can often involve a radical shift in the mating system of the new population relative to the ancestral one. For sexually selected traits, random genetic drift coupled with sexual selection can act as a particularly powerful mechanism for driving speciation (Lande, 1981; Boake, 2005).

B. Founder Effect Consequence for Biogeography

Biogeography starts at the colonization event. The term “founder effect” was first introduced by Mayr (1954) to describe the genetic accidents inherent in small population size that may be important during colonization. To explain the divergence of peripheral populations, Mayr (1954) proposed that genetic change throughout the genome could be extremely rapid in small localized populations that are founded by a few individuals (genetic drift) and are cut off from gene exchange with the main body of the species. Moreover, the selective pressures acting on the population are likely to be different, because the environment of a small peripheral region might present different characteristics. Both neutral and selective processes can induce changes in the genetic structure of isolated populations, and the use of both markers under genetic selection (allozymes) and neutral ones (microsatellites) would allow us to characterize evolutionary processes driving genetic differentiation.

In the late 1950s and early 1960s the Bureau of Commercial Fisheries, at the request of the Division of Fish and Game of the State of Hawaii, undertook an introduction program, which was supposed to import new species of groupers and snappers for fisheries purposes. Such official programs of introduction of new species provide unique opportunities to follow in situ founder effects in terms of genetic evolution. Between 1955 and 1961, 11 species of Serranidae and Lutjanidae were introduced from several geographic locations. Among these species only 3 are known to be established (Oda and Parrish, 1981; Randall, 1987a):

Cephalopholis argus is a widespread grouper that occurs from the east coast of Africa to French Polynesia. In 1956, 571 small individuals were transported from Moorea (Society Archipelago) to the Hawaiian Islands. One lot of 171 was released in Oahu and the remaining 400 were released in Hawaii (Big Island). This fish has not become abundant and it is encountered mainly in Hawaii.

Lutjanus fulvus occurs throughout the Indo-Pacific region. A first introduction in 1956 brought 239 individuals from Moorea to Kaneohe Bay in Oahu. About 3000 additional individuals from the Marquesas Islands were subsequently introduced in the bay. This species became established in Oahu and spread to all other islands of the Hawaiian Archipelago.

In 1958, 2435 Lutjanus kasmira were transported from the Marquesas Islands and released in Kaneohe Bay. The blue-lined snapper has spread throughout the Hawaiian Islands and reaches high abundance in some places. Because of its high abundance and its consequent competition with native species, Randall (1987a) considered this introduction as an unfortunate one.

Such introduction programs can be viewed as founder effects from a population genetics perspective because, for the species that became established, the population started from a small number of individuals.

Despite the fact that only 571 C. argus and 2435 L. kasmira were released, no major change in polymorphism and heterozygosity was observed between ancestral and introduced populations (Planes and Lecaillon, 1998). However, the change in allelic frequencies allows an estimate of the effective population size for the Hawaiian Islands populations of between 1 and 5% of the total population size. Such reduced effective population size explains why most of the species introduced in Hawaii (8 out of 11) failed to establish. These planned introductions also permit a test for the selective neutrality of allozymes under extreme conditions—the transport of fish from French Polynesia to Hawaiian Islands must involve a significant change in environment. Comparisons of raw data to models including selective change suggest that the difference observed over the short period since introduction should lead to fixation of alleles within 60 to 200 generations. This seems unlikely when looking at polymorphism found in other Hawaiian species (Shaklee, 1984; Shaklee and Samollow, 1984).

The establishment of introduced species appears to be determined by some sort of lucky event that will favor the reproduction of adults and the return of oceanic larvae. This result suggests that colonization events may occur more often than we expect, but that the establishment of the new species into a new biogeographic area is less frequent. Success of the first reproductive events in a small population appears to be hazardous. Certainly, many species have managed to colonize new areas and modern species distributions are a result of those species that managed to establish at a site because they colonized, found a suitable adult habitat, and were able to use the surrounding ocean to complete the life cycle.

Genetic Drift

Differential pollen and seed production means a ‘random genetic sampling’ of the parent population. The smaller the sample, the more the offspring depart from the Hardy–Weinberg allelic ratios. If the population size remains low, drift recurs every generation. Drift effects may persist long after the population regains its size, if the original allelic richness is not replenished through gene flow, e.g., after a demographic bottleneck (through a catastrophic fall in numbers), or if very few individuals colonize a new habitat (founder effect). For example, the loss of alleles during postglacial recolonization is still evident in many temperate species, despite gene flow over many generations.

Figure 8 shows that diversity loss in small populations depends on the effective number of population members. Through random fluctuations, alleles might be lost or fixed even if their initial frequencies were high or low respectively.

As a result, small populations typically show an excess of homozygotes due to a higher number of fixed (monomorphic) loci. Random fixation of some deleterious alleles (harmful mutants) is also probable if the effective number is small or if selection pressure (s) is mild. At the species level, drift in single fragmented populations does not necessarily lead to loss of diversity and may even increase among-population additive variance. For example, in island populations of sugar maple (Acer saccharum), fragmented by agricultural fields, polymorphism was found to be higher than in closed, large stands.

Genetic drift may be compensated by gene flow. Model calculations show that relatively low migration rates suffice to offset drift effects. The maintenance of gene flow between scattered stands is therefore important for avoiding divergence of species fragments.

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