The Ecological Genetics of Introduced Populations of the Giant Toad, Bufo Marinus. IV. Gene Flow Estimated from Admixture in Australian Populations
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Heredity 56 (1986) 145—156 The Genetical Society of Great Britain Received 24 May 1985 The ecological genetics of introduced populations of the Giant Toad, Bufo marinus. IV. Gene flow estimated from admixture in Australian populations Simon Easteal Department of Population Biology, Research School of Biological Sciences, The Australian National University Canberra, A.C.T. 2601, Australia. Allele frequency variation is described at nine polymorphic enzyme loci in 21 samples from populations of the introduced Giant Toad, Bufomarinus,in the region of Townsviile in north Queensland, Australia. Some of these populations appear to have been established through the introgression of other populations that previously had been isolated. Comparisons of allele frequencies at three polymorphic loci between the introgressed populations and the original populations are used to obtain admixture estimates. These are used to estimate a rate of gene flow among the populations of approximately 2 km/year. This is consistent with an estimate based on the rate at which Bufomarinus has colonised new areas in Australia when discontinuities in the pattern of this colonisation are taken into account. The estimate of gene flow is combined with published data on population density to estimate neighbourhood size. The estimate obtained is substantially greater than the effective population size estimate determined previously from data on allele frequency variances in other populations. This discrepancy is most likely due to inaccuracies in the population density estimates, to underestimates of the extent of offspring number variance and perhaps to occasional departures from sex ratio parity. It has important implications for the study of the genetic structure of populations which are discussed. INTRO DUCTI ON Koehn, 1978; Daly, 1981; Zera, 1981). The third approach is suggested by Slatkin (1981), who Generalisationsabout gene flow and its import- showed that an allele's average frequency among ance as a cohesive force in evolution (Mayr, 1963; local populations, conditioned by the number of Ehrlich and Raven, 1969; Stanley, 1979) have little local populations in which it occurs, is largely empirical basis. Direct estimation of gene flow has independent of selection intensity and mutation been achieved in few species and then only on a rate, but is strongly dependent on gene flow (tn) limited scale (Schaal, 1980; Handel, 1983; Baker, and effective population size (Ne). This "condi- 1981; Singleton and Hay, 1983). The difficulties tional average allele frequency" (pt) can be used usually encountered in attempting direct estima- as an estimate of the compound parameter Nem, tion have led most workers to use indirect methods. as demonstrated by Larson et a!. (1983). There have been three general approaches. In the There are problems with all three of these first, the dispersal of individuals is determined on approaches. The relationship between dispersal the assumption that the movement of individuals and gene flow may be complicated by the breeding is approximately equivalent to the movement of and social behaviour of the species and for this genes (e.g.,Endler,1977; Gill, 1978; Jones et a!., and other reasons, discussed by Endler (1977), it 1981; Patton and Feder, 1981; Coyne et a!., 1982; is generally supposed that gene flow is spatially McCauley, 1983). The second approach involves restricted in relation to dispersal, at least in animal the estimation of the standardised variance (FST) species. The extent to which this is the case has of gene frequencies among populations, on the not been determined in any particular instance, assumption that this is a function of the extent of but estimates of dispersal will tend generally to be gene flow between them (Endler, 1977; Eanes and overestimates of gene flow. Allele frequency vari- ances are affected by population size and by Present address: Department of Zoology, The University of natural selection as well as by gene flow. Only Oklahoma, Norman, Oklahoma 73019, U.S.A. when the effective sizes of populations are known 146 SIMON EASTEAL and the effects of selection are either known, or Allele frequencies were weighted for sample can be assumed to be negligible, can the extent of size in calculating their means and variances. The gene flow be inferred from allele frequency vari- genetic identities (I) and genetic distances (D) ances among populations. Similarly, the condi- between populations were calculated by the tional average allele frequency depends on both method of Nei (1978). Populations were clustered effective population size and gene flow, and gene in dendrograms of genetic relatedness using the flow cannot be determined from estimation of p, unweighted pair group method of Sneath and without an independent estimate of Ne. Sokal (1973). The computer program BIOSYS In human populations gene flow has been esti- (written by D. L. Swofford and R. B. Selander) mated directly by studying the changes in gene was used in estimating I and D and in the construc- frequencies which result from admixture of pre- tion of the dendrograms. viously isolated, genetically different populations, particularly of Caucasians, Amerindians and Blacks in North and South America (e.g., HISTORICALBACKGROUND Workman,1973; Ward and Neel, 1976; Crawford etal., 1981;Franco etal.,1982). This approach is made possible by the availability of information B.marinus was introduced to Australia from on the demographic history of these populations. Hawaii in 1935 and by 1937 had been released Such information usually does not exist for popu- throughout the sugar-cane growing districts of lations of other species, so that the approach has Queensland (Easteal, 1981). Sabath et a!. (1981), not been applied except to humans. Easteal eta!. (1985) and Easteal and Floyd (1985) I apply the approach here to populations of have described the subsequent spread of the the neotropical Giant Toad, Bufo marinus, whose species in Queensland, based on distribution and introduction and spread in Australia have been first sighting records compiled by Floyd et a!. well documented. Admixture is determined in (1981). Large numbers of toads are known to have populations in the Townsville region of north been released in the Ingham/Bambaroo and Queensland, that appear to lie between three popu- Giru/Ayr districts between 1936 and 1937 lations established in isolation from each other 35 (Mungomery, 1937). These districts are approxi- to 40 years ago, and which were formed as these mately 100 kilometres north-north-west and 50 earlier established populations expanded towards kilometres south-east of Townsville respectively. each other and merged. The admixture estimates Floyd et a!. (1981) record sightings of B. marinus will be used to infer rates of gene flow. in both districts in or before 1940, confirming that The gene flow estimate presented here will be populations were successfully established from discussed in relation to the rates at which B. both releases. Toads were first seen in Townsville marinus has dispersed into new areas in Australia at Mundingburra in 1944 and at Pimlico in 1945. (Easteal and Floyd, 1985) and to estimates of the These are adjacent suburbs, north of the Ross effective size of B. marinus populations in Hawaii River, in the city of Townsville. There are no and Australia (Easteal, 1985a). reported sightings from the areas directly between either Ingham/Bambaroo and Townsville or between Giru/Ayr and Townsville until 1974. In MATERIALSAND METHODS 1948 there were sightings at Calcium and Reid River to the south of Townsville (fig. 1). One-thousand,nine-hundred and seventy-four It can hence be presumed that B. marinus was toads were collected in 1979 and 1980 from 21 established in Townsville by 1944-45 and in the localities in the area of Townsville. Specimens were Calcium/Reid River area by 1948. Although we transported live to the laboratory where they were do not know the sources of either population, both killed either by pithing or freezing. All methods localities are closer to the Giru/Ayr district than of tissue preparation, electrophoresis and his- to any of the other districts in which B. marinus tochemical staining are as described in Easteal was originally released or in which it occurred (1982; 1985a). All explanations of locus nomen- before 1945. It seems most likely therefore that the clature and its abbreviation can also be found in Townsville and Calcium/Reid River toads are these other publications. Electrophoresis was per- derived from the Giru/Ayr population. It is not formed using horizontal 12 per cent starch gels or however critical to assume this in the analyses that cellulose acetate plates. follow. GENE FLOW IN BUFO MARINUS 147 PACIFIC OCEAN MAGNETIC ID. Figure 1 Diagram of study site, showing position of sample localities (1-21), location and dates of first sighting recordsof Bufo marinus, and the main geographical features of the area. 148 SIMON EASTEAL RESULTS localities, separated by only a few kilometres. It seems unlikely that greater selective regime Allele frequency variation differences exist between the Magnetic Island and Twenty-oneloci were scored. Twelve of these were mainland populations than among the Hawaiian monomorphic in all 21 populations. The allele and other Australian populations; unlikely there- frequencies of the remaining nine polymorphic loci fore that the Magnetic Island differences have are listed in table 1. At several loci, particularly resulted from the differential effects of natural Iddh, Mdh : NADP, and Sod, there are large allele selection. frequency differences between the Magnetic Island Among the mainland populations there is also population (1) and all other populations. It seems allele frequency variation. This was estimated as likely that these differences arose substantially as sT= u2/(1 —), wherecr2 is the variance of allele a result of genetic drift associated with a popula- frequencies among populations (corrected for tion size bottleneck which occurred at the time the sampling error variance as described by Easteal, toads were introduced to the island, rather than 1985 a) and is the mean allele frequency among through the action of natural selection.