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The Speciation History of Drosophila Pseudoobscura and Close

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The Speciation History of Drosophila Pseudoobscura and Close Copyright 0 1996 by the Genetics Society of America The Speciation history ofDrosophila Pseudoobscura and Close Relatives: Inferences from DNA Sequence Variation at the Period Locus Rong-Lin Wang' and Jody Hey Department of Biological Sciences, Rutgers University, Piscataway, NewJersey 08855-1 059 Manuscript received June 3, 1996 Accepted for publication August 3, 1996 ABSTRACT Thirty-five period locus sequences from Drosophila pseudoobscura and its siblings species, D. p. bogotana, D. persirnilis, and D.rniranda, were studied. A largeamount of variation was found within D. pseudoobscura and D.persirnilis, consistent with histories of large effective population sizes. D. p. bogotana, however, has a severe reduction in diversity. Combined analysis of perwith two other loci, in both D.p. bogotana and D. pseudoobscura, strongly suggest this reduction is due to recent directional selection at or near per within D.p. bogotana. Since D. p. bogotana is highly variable and shares variation with D.pseudoobscura at other loci, the low level of variation at perwithin D. p. bogotana can not be explained by a small effective population size or by speciation via founder event. Both D. pseudoobscura and D. persirnilis have consider- able intraspecific gene flow. A large portion of one D.persirnilis sequence appears to have arisen via introgression from D. pseudoobscura. The time of this event appears to be well after the initial separation of these two species. The estimated times since speciation are one mya for D. pseudoobscura and D. persirnilis and 2 mya since the formation of D. miranda. VOLUTIONARY biologists areconcerned with One of the best studied species groups includes Dro- E both the population genetic mechanisms behind sophila pseudoobscura and its close relatives:D. persirnilis, evolutionary processes and the reconstruction of phy- D.miranda, and subspecies D.p. bogotana. D.pseudoobsc- logeny. The study of speciation is at the interface of ura and D. persirnilis were once thought to be a single these two areas of investigation. Knowledge of specia- species but were later differentiated from each other tion is fundamental to our understanding of how the based primarily on different chromosome arrange- biological landscape grows and changes at a macrolevel. ments and nearly complete sexual isolation (DOBZHAN- Yet it is the forces at the microlevel, including mutation, SKYand EPLING1944). Females ofboth species discrimi- migration, random genetic drift, and natural selection, nate against heterospecific maleswhile males court that lead to speciation. females of either species (MAYR 1946). Crossed under Speciation, as a genetic process, can be studied from laboratory conditions in either direction,they generate two different empirical perspectives. First are studies of sterile males but fertile females. There is some chromo- the genetic basis of species differencesand of reproduc- some inversion (DOBZHANSKY1973) and mitochondrial tive barriers among species. These types of studies are DNA data (POWELL 1983; HALEand BECKENBACH1985) focused on the number and identity of loci at which that suggest some degree of gene flow between these divergence may have, in some sense,contributed to speci- two species. ation (Wu and PALOPOLI1994). Whilecritically im- Later came the discovery of D. miranda (DOBZHANSKY portant, these analyses do not inform on the historical 1935) and D. pseudoobscura bogotana (DOBZHANSKYet al. microlevel forces associated with speciation. A different 1963), anisolated population in Bogota, Columbia. Re- perspective can be gained by studying patterns of DNA productive isolation between D. miranda and its sibling sequence variation, withinand among closely related spe- species is essentially complete (DOBZHANSKYand cies, at loci that may or may not have been associated EPLING1944) but that between D. pseudoobscura and D. with species formation. This approach is essentially an p. bogotana is not: female D.p. bogotana crossed to male extension of traditional population genetic questions to D. pseudoobscura giverise to sterile males and fertile distant time periods, and it is made possible by a recent females (PRAKASH1972). synergism between genealogicalpopulation genetic mod- D.pseudoobscura has the widest range of geographic els and studies on DNA sequence variation (see e.g, AVISE distribution within the group, extending from British and BALL 1990; HEY1994; TEMPLETON 1994). Columbia, along thewestern third of the North Ameri- can continent, to Mexico and Guatemala. D. persirnilis Cmespondzng author:Jody Hey, Department of Biological Sciences, and miranda are sympatric to pseudoobscura and Rutgers University, Nelson Labs, P.O. Box 1059, Piscataway, NJ 08855 D. D. 1059. E-mail: [email protected] found in the mountain ranges along the US. Pacific 'Present address: Department of Plant Biology, University of Minne- Coast. Morphological, chromosomal, and molecular ev- sota, 1445 Gortner Ave., St. Paul, MN 55108-1020. idence indicate that D.pseudoobscura is most closely re- Genetics 144: 1113-1126 (November, 1996) 1114 R.-L. Wang and J. Hey TABLE 1 A list of samples and their geographic origins Species NDSRC" lines Sample numbers Locations D. pseudoobscura 0121.0 1 Tucson, A2 0121.1 2 Death Valley, CA 0121.33 3 Kelowna, British Columbia 0121.34 4 Cuernavaca (Mexico) 0121.38 5 Mather, CA 0121.41 6 Mather, CA 0121.37 7 Mather, CA 0121.32 8 Zimapan, Hidalgo (Mexico) 0121.78 9 Dilley, TX 0121.79 10 Port Coquitlam, British Columbia, Canada 0121.83 11 Spray, OR D. miranda 0101.4 22 Port Coquitlam, British Columbia 0101.3 23 Port Coquitlam, British Columbia 0101.5 24 Port Coquitlam, British Columbia 0101.7 25 Port Coquitlam, British Columbia D. persirnilis 0111.0 40 Cold Creek, CA 0111.2 41 Mt. San Jacinto, CA 0111.17 42 Port Townsend, Washington 01 11.23 43 Victoria, British Columbia 0111.24 44 McDonald Ranch, CA 0111.1 45 Quesnal, Canada 0111.18 46 McDonald Ranch, CA 0111.27 47 Mt. San Jacinto, CA 0111.29 48 Mt. San Jacinto, CA 0111.35 49 Mt. San Jacinto, CA 0111.38 50 Victoria, British Columbia D. p. bogotana 0121.35 60 Bogota, Columbia 0121.68 61 Bogota 0121.69 62 Bogota 0121.71 63 Bogota Oicata 9A 67 Bogota Sutatausa 4 70 Bogota Chiquinquira A 73 Bogota A Cacientes 4C 74 Bogota EL Recreo 77 Bogota National Drosophila Species Resources Center (Bowling Green, OH) lated to D.p. bogotana, and together, they share a com- POWELL1992). To date there has not been a nuclear mon ancestor with D. persirnilis (GODDARDet al. 1990). gene DNA sequence study on variation in D. persirnilis. D. rniranda is an outgroup to all other three species. Our study has focused on a 1.5-kb portion of the Together, D. pseudoobscura and its close relatives have period locus (per). Per is an essential component of the beenthe subject of vigorous population genetic re- biological clock in D. rnelanogaster (KONOPKAand BEN- search for several decades (LEWONTINet al. 1981). At ZER 1971; ROSBASHand HALL 1989; EDERYet al. 1994) the DNA level, much of the focus has been on D.pseudc- and found to occur as a single copy gene on the X obscura and onthe relationship between D. pseudoobscura chromosome. Per is also involved in the determination and D. p. bogotana. D. pseudoobscura is clearly a species of male courtship songs (Kmcou and HALL 1980, with a large historical effective population sizewith 1989; Kmcou 1990) which in turn affect the female ample gene flow across much of its range (RILEY et al. response to male mating attempts (KYRIACOUand HALL 1992; SCHAEFFERand MILLER1992; VEUILLEand KING 1982, 1984; K~COUet al. 1992). Per thus appears to 1995). There is also strong evidence for the action of be a candidate for evolutionary changes in mating be- natural selection acting on third chromosome inversion havior that contributeto reproductive isolation and spe- polymorphisms (AQUADROet al. 1991; POWELL1992). ciation. However, in the rnelanogaster species complex, D. pseudoobscura and D. p. bogotana share considerable there is no evidence that variation at perhas contributed DNA sequence variation at the Alcohol dehydrogenase to reproductive isolation or to species divergence (KLI- locus (Adh either because of ongoing gene flow or re- MAN and HEY 1993;RITCHIE and KYRIACOU1994). Re- cent divergence or both (SCHAEFFERand MILLER1991; gardless of whether evolution at per contributes to re- Speciation 1 D. psevdoohscura Speciation 115 exon II 111 IV V VI VI1 Vlll "threonine - glycine"- like repeats j/ * _,. FIGURE1.-Diagram of the period locus! D. "z psmdoohscurn, based on COI.OT rt al. 1988. bp total 4 4763 b -1.5 kb sequenced productive isolation, a study of sequence variation estimate of the population recombination parameterwas ob- within and amongclosely related species can yield valu- tained using the method of HUDSON(1987). Theestimate of able information on species divergence. divergence times among the species is based on the substitu- tion rates at synonymous sites (SHARP andLr 1989). The primary objective of this studyis to gain a genea- Outlier HKA test: The HKA test of natural selection is simi- logical perspectiveof the population genetic forces asso- lar to a chi-square test and asks whether the relative levels of ciated with the formation of the two sibling species, D. intraspecific polymorphism and interspecific divergence for pseudoohscura and D. pmirnilk, as well as the geographi- a locus, are consistent across loci (HUDSONel al. 1987). The first step in applying the test is to complete a table that has, cally isolated subspecies, D. p. boptana. Assessments of for example, as many rows as there are loci in the data set DNA sequence variation can reveal relative historical ef- and three columns: one for variation in one species, one for fective population sizes, and the patterns of shared varia- variation in the second species, and one for the divergence tion may be used to aSsess historical levels of gene flow between species. Like a chi-square test, the test proceeds by within and between species (HUDSONet al.
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