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Home , Allopatric speciation, Drosophila silvestris, Peripatric speciation

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Allopatric and sympatric modes of : examples from

B. N. Singh* Laboratory, Department of Zoology, Institute of Science, Banaras Hindu University, Varanasi 221 005, India

, which was ‘Reproductive community of sexually Basically, there are two different ways by which new species are created: and (true or cross fertilizing individuals which share in a common ’7. Evolutionary was suggested speciation). During anagenesis, one species is trans- 8 formed into new one so there is a phyletic change in by Simpson who considered species as a lineage (ance- 9 the course of time and there is no involvement of stral-derived relationship), but it was criticized by Mayr . Cladogenesis is considered as who denied it as the definition of species, but that of true speciation during which new species originate phyletic lineage which was also applicable to incipient through splitting of pre-existing ones. Different species. There are more than twenty species concepts models have been proposed from time to time to suggested by naturalists, evolutionary biologists and taxo- explain the modes of speciation. There are two impor- nomists1,2,10. Darwin11 who proposed the tant modes of speciation which are primarily based on theory of to explain the mechanisms of evolu- geographic factors: allopatric (dichopatric and peri- tion, was initially a supporter of BSC but later supported patric) and sympatric. In this article, both allopatric morphological species concept which was related to his and sympatric modes of speciation are briefly 12 13 described with the help of suitable examples from theory of natural selection . Mayr introduced the con- Drosophila. cept of sibling species for those species which were morphologically similar but reproductively isolated. In

Drosophila, a large number of sibling species (pairs or Keywords: Allopatric, Drosophila, speciation, sympa- groups) showing evolutionary significance have been re- tric. ported14. Cook15 coined the term speciation during which

new species of arise. Different evolutionary SPECIES is a taxonomic rank and it is also the basic unit biologists have suggested different modes of specia- of binomial classification. There are a large number of tion3,4,13,16–21. The terms used in this article are explained, concepts of species which define them in different which are: Allopatry – species living in different geo- ways1,2. Linnaeus (1707–1778), a prominent taxonomist graphical areas; – species living in the same suggested the binomial nomenclature and was a strong geographical area; – random fluctuation in supporter of typological species concept (essentialism). frequency in small ; Founder effect – Mayr and Ashlock3 have described four species concepts: when a daughter species arises from a few individuals (in typological, nominalistic, biological and evolutionary extreme case a single gravid female), there will be a larger species concepts in their book Principle of Systematic founder effect; Asymmetrical mode of sexual isolation – Zoology. The most widely accepted concept is biological between two species when sexual isolation is one-sided, species concept (BSC) which has been elaborated in de- it is called asymmetrical isolation, and when sexual isola- tail by Jordan, Mayr and Dobzhansky2. Different species tion is two-sided, it is called symmetrical isolation; Ance- concepts and modes of speciation have also been dis- stral-derived species – when the original species giving cussed by Singh2. Coyne and Orr4 suggested that defini- rise to another (new) species, the former is ancestral spe- tions of species have been historically controversial but cies and the new one is derived species; Stabilizing, cen- one of the most widely accepted concept is BSC. Accord- tripetal or normalizing selection – it signifies selection ing to Castillo and Barbash5, BSC works well for Droso- for intermediate and elimination of extreme phila for the study of evolution of reproductive isolation, phenotypes, which leads to reduction in the degree of but other species concepts may have more utility for taxo- genetic variability; Disruptive selection or diversifying nomic and systematic studies. Mayr6 defined a species as selection is, when a is subjected within a ‘Group of actually or potentially interbreeding natural single generation to various environments to which populations which are reproductively isolated from other different are most suited and this leads to sus- such groups’. Dobzhansky was a population geneticist tain the genetic variability. Different factors have been and introduced the term gene pool to the definition of considered important in the process of speciation such as mechanisms generating genetic variability, origin of *e-mail: [email protected] reproductive isolating mechanisms and geographical

56 CURRENT SCIENCE, VOL. 121, NO. 1, 10 JULY 2021 REVIEW ARTICLES factors. On the basis of these factors, White16 proposed between them. Both subpopulations which are allopatric different models to explain the modes of cladogenesis in distribution, evolve independently due to the action of (true speciation) like: (i) Strict allopatry without a narrow different evolutionary forces such as , natural population bottleneck, (ii) Strict allopatry with a narrow selection, genetic drift, migration, etc. and accumulate population bottleneck (founder effect), (iii) of micro-evolutionary changes in the long course of time. intermediate populations in a chain of races, (iv) Clinal Because of geographic isolation, between them speciation, (v) Area effect speciation (primarily genic), is completely prevented and they become genetically dif- (vi) Stasipatric speciation (primarily chromosomal), and ferent. In the long run, they develop genetically based (vii) . White16 considered mechanisms of reproductive isolation and acquire the sta- which is basically a chromosomal model separately, and tus of two separate allopatric species. If the geographic comes under sympatric mode of speciation that common- barrier is removed, they become two sympatric species ly occurs in plants. Mayr13 gave much emphasis on geo- but interbreeding is prevented between them since they graphic speciation (allopatric) which is an important would have already developed reproductive isolating mode of speciation. Thus, two are primarily mechanisms. Thus, allopatric species become sympatric important namely, allopatric and sympatric, during which species due to removal of geographical barrier, and still new species of organisms arise due to origin of reproduc- maintain their own gene pool due to prevention of inter- tive isolating mechanisms which are considered a breeding. Thus, allopatric species originating through pre-requisite for speciation22. Sexual isolation which is a dichopatric mode of speciation (dumbbell model) become prezygotic (premating) isolation has been extensively sympatric because of the developing zone of contact studied in Drosophila, and the asymmetrical mode of resulting from the removal of geographical barrier. One mating preference is considered to discuss ancestral– example of dumbbell model of is derived relationship between species which are primarily provided in when the population based on allopatric and sympatric modes of specia- existing at low elevation had been split into two by the tion23,24. Nanda and Singh25 discussed the behavioural re- separation of two Molokai from Maui due to rise productive isolation and speciation in different species in sea level16. groups of Drosophila including Hawaiian species along In the allopatric mode of speciation (with a narrow with origin of sexual isolation, genetics of premating iso- population bottleneck), which is also known as peripatric lation, asymmetrical mode of mating preference, and the mode of speciation, a small number of individuals (in direction of evolution. In this article, both allopatric and extreme case a single gravid female) migrate from the sympatric modes of speciation are discussed briefly with original population to a new area and evolve into a new suitable examples from Drosophila which is considered species in the long course of time. It becomes genetically as an interesting and important biological model. different from the original population as it passes through population bottleneck/founder effect/flush crash cycle. It has also been suggested that the rate of evolution is faster Allopatric mode of speciation in such cases because of the action of genetic drift and genetic differences. This is the basic difference between Based on geographical distribution of species/popu- dichopatric and peripatric modes of speciation although lations, different terms are used such as sympatric, broadly both come under allopatric mode. Carson26–29 did allopatric, parapatric and peripatric. To explain the extensive work on Hawaiian species of Drosophila and mechanism of speciation, geographical component is very explained their evolution by peripatric mode of speciation important. It may range from absence (sympatric) to involving population bottleneck, founder principle, ran- complete separation (allopatric). Allopatric mode of spe- dom genetic drift and flush crash cycles. In the Hawaiian ciation was initially called geographic speciation by Islands, there are more than 500 species of Drosophila Mayr13,18 who believed that it was the most important distributed on different islands and their evolution has mode of speciation. Whereas other evolutionists used the been explained by founder principle. There are about 100 term ‘allopatric’ mode of speciation4,16,21. Basically allo- picture winged Drosophila species which have been uti- patric speciation is of two types: dichopatric or dumbell lized for evolutionary, behavioural and cytogenetic stu- model and . There is a sharp differ- dies23,30,31. Kaneshiro23,32 studied certain aspects of ence between these two types. In dichopatric, there is no behavioural isolation in certain species of picture winged role of genetic drift or population bottleneck or founder Hawaiian Drosophila. Based on asymmetrical mode of principle. However, in the peripatric speciation, there is a sexual isolation (one-sided sexual isolation), Kaneshiro23 profound effect of genetic drift/population bottleneck/ suggested the direction of evolution among the species of founder principle. In dichopatric mode of cladogenesis, a D. planitibia subgroups: D. differens, D. planitibia, D. population of species splits into two subpopulations heteroneura and D. silvestris. Based on the asymmetrical which are of large size separated by geographical/eco- mode of mating preference, he suggested that the ance- logical barriers having no contact and no gene flow stral females discriminate against derived males because

CURRENT SCIENCE, VOL. 121, NO. 1, 10 JULY 2021 57 REVIEW ARTICLES of loss of certain courtship elements of males due to ran- bristle phenotypes did not produce ethological isolation dom genetic drift. His model is also based on genetic drift between high and low lines’ , as the pattern of mating (founder effect) causing allopatric mode of speciation. between the two types was random. However, this Origin of asymmetrical sexual isolation in drift lines with affected the mating propensity of flies in different selec- varying number of founders has been reported in D. ana- tion lines, i.e. high line flies had high mating propensity nassae33. The phylogenetic relationship between the and the low lines showed low mating success. Thus, the species/strains based on asymmetrical mode of mating results of D. ananassae did not support the observation preference has also been suggested to support Kaneshi- reported in D. melanogaster39. ro’s model34–38. Thus, the findings on these species sup- Watanabe and Kawanishi24 suggested a hypothesis port the role of genetic drift in speciation extending which was just opposite to that of Kaneshiro’s, to explain evidence for allopatric mode of speciation. the direction of evolution based on asymmetrical mode of mating preference. They studied sexual isolation among D. melanogaster, D. simulans and D. mauritiana and Sympatric mode of speciation found one-sided sexual isolation between them. Accord- ing to their model, the derived females discriminated Sympatric mode of speciation has been explained by against the ancestral males24. The concept24 given by different evolutionary biologists4,16,20,21. Singh2 also re- them has been used to discuss the evolutionary sequence viewed species concepts and modes of speciation with the of species in different species groups of Drosophila. help of various examples. In the same geographical area, Watanabe and Kawanishi24 proposed that the failure of new species originates from the segments of the original mating between females of new species and males of an- population through instantaneous origin of reproductive cestral species was the first step in developing reproduc- isolation. Both species remain in the same geographical tive isolation and creation of incipient species favouring area and maintain their integrity. These species are called sympatric mode of speciation41. They also suggested that sympatric species. However, when they are separated, the genes of new populations, if found in ancestral popu- and one or both species move to other areas, they are lations due to some matings between females of ancestral called allopatric species. Thus, in the sympatric mode of species with the males of derived ones, are eliminated speciation, the most important factor is the instantaneous through the action of stabilizing selection24. One-sided origin and development of certain reproductive isolating mating preference has been found between D. bipectinata mechanisms between the segments of original population and D. parabipectinata, where D. bipectinata is consi- and parental population in the same geographical area. dered ancestral to D. parabipectinata because females of Hence, it has been stated that the reproductive isolating D. parabipectinata discriminate against the males of D. mechanisms are pre-requisites for speciation22. Several bipectinata. This favours Watanabe and Kawanishi’s hy- examples demonstrating the occurrence of sympatric pothesis42,43. Asymmetrical mating preference between mode of speciation are described by White16. Polyploidy, isofemale lines of D. ananassae44 as well as light (palli- which is a more common means of speciation in plants dosa) and dark (ananassae) forms of D. ananassae45,46 also comes under this mode. As far as Drosophila is con- have also been explained by Watanabe and Kawanish’s cerned, a very good example was cited from the laboratory model, as derived females discriminate against ancestral experiments on disruptive selection in D. melanogaster39. males41. Thus D. ananassae (dark form) is considered Selection was done for high and low number of sternop- ancestral to D. pallidosa (light form). Both these species leural bristles in D. melanogaster for several generations. are sympatric in distribution and their separation is main- In each generation, tests were carried out to determine the tained by ethological isolation. D. ananassae is a cosmo- type of progeny produced by forced high–high, high–low politan and domestic species whereas its sibling D. and low–low matings. It was confirmed by these tests that pallidosa has localized distribution in south central Paci- the absence of flies with intermediate number of sternop- fic islands of Samoa and Fiji46. These examples support leural bristles after several generations was due to repro- the sympatric mode of speciation41. Dobzhansky47 gave ductive isolation between two types of flies. It was an importance to natural selection in sympatric populations interesting experiment demonstrating the occurrence of for of incipient species. Figure 1 de- sympatric speciation in a laboratory. Disruptive selection picts the different modes of speciation during which new for sternopleural bristle number in D. melanogaster pro- species originate in the course of time due to the origin of duced divergence for both sexual isolation and the bristle genetically based reproductive isolating mechanisms. A number simultaneously. Thus, the development of sexual population of a species may give rise to two separate (behavioural or ethological) isolation due to disruptive species characterized by prevention of gene flow which selection in the laboratory demonstrated the role of sym- may be sympatric or allopatric depending upon their geo- patric speciation in D. melanogaster16. Nanda and Singh40 graphical distribution. During the process of cladogenesis conducted similar experiments in D. ananassae for 12 (true speciation), all the three components are important generations, but disruptive selection for sternopleural namely, geographical factor, genetic variability and

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Figure 1. Schematic representation of (a) Sympatric, (b) Allopatric without a narrow population bottleneck and (c) Allopatric with a narrow population bottleneck (peripatric/founder effect) modes of speciation (modified from Bush20 and Savage48). The geographical component and development and perfection of reproductive isolating mechanisms are impor- tant for the origin of species.

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