The Journal of Heredity 2002:93(6)
© 2002 The American Genetic Association 93:415-420
Strong Founder Effect in Drosophila pseudoobscura Colonizing New Zealand from North America
From the Department of Biological Sciences, 202 Life Sciences, Louisiana State University, Baton Rouge, LA 70803 (Reiland and Noor), and Department of Entomology and Nematology, IACR-Rothamsted, Harpenden, Hertfordshire, UK (Hodge).
Address correspondence to Mohamed A. F. Noor at the address above, or e-mail: mnoor{at}lsu.edu.
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Abstract |
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The North American native species Drosophila pseudoobscura was first identified in New Zealand in the last few decades. Here, we have studied the genetic consequences of its spread across the Pacific Ocean. Using 10 microsatellites that are highly variable in North American populations, we found that the New Zealand population has substantially fewer alleles, a much lower average heterozygosity, and significantly different allele frequencies at these loci. We have discussed the relative sensitivity of these parameters for detecting the founding event. X-linked loci were more strongly differentiated between continents than autosomal loci, as reflected by larger changes in allele frequencies and greater reductions in numbers of alleles and average heterozygosity. The severity of the genetic diversity loss supports a scenario of a few D. pseudoobscura females being introduced to New Zealand from North America.
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Introduction |
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New Zealand has been the site of recent colonization by many species, including various birds (Ardern et al. 1997; Merila et al. 1996), wallabies (LePage et al. 2000), salmon (Quinn et al. 1996, 2001), and pests (Gleeson 1995; Nicol et al. 1998). The introduction of these species has had profound impacts on the native flora and fauna (Wardle et al. 2001). In many of these cases, the means of introduction of these species is unknown, but there exists genetic evidence for a recent "founder effect." Founder effects generally result in divergence between the ancestral and the founded populations, typically reflected in three types of genetic data: a decrease in heterozygosity, loss of alleles, and changes in allele frequencies. These signatures of founder effects have been documented by examining DNA sequences, allozymes, restriction fragment length polymorphisms (RFLPs), and microsatellites.
Genetic studies of founder effects in species for which the timing of colonization is known can be informative, and results from such studies may lead to improved hypotheses of how to interpret resultant changes in genetic variation. Microsatellites are useful markers for accessing the genetic variation in populations (Luikart and England 1999). Several studies have shown that changes in allelic frequency and allelic loss are more powerful measures for detecting bottlenecks than the traditional use of heterozygosity (Allendorf 1986; Luikart et al. 1998b; Spencer et al. 2000). Luikart et al. (1998b) compared loss of heterozygosity, loss of alleles, change in the variance of allele frequencies, and changes in allele frequency distributions to detect recent bottlenecks. They found that allelic loss and variance in allelic frequency were most sensitive for identifying recent bottlenecks, while heterozygosity was relatively insensitive. However, analyses of microsatellite data in experimentally induced founder events suggest that expected heterozygosity can also be useful for detecting recent bottlenecks (Spencer et al. 2000).
Here we report the results of a genetic study of the spread of Drosophila pseudoobscura to New Zealand. Endemic to North America, D. pseudoobscura invaded New Zealand sometime in the 20th century, probably within the last 50 years. Individual obscura-group flies were reported by Harrison (1959) and Parsons (1982) earlier this century. In contrast to D. pseudoobscura from South America, these flies are cross-fertile with North American D. pseudoobscura (Millar and Lambert 1985), suggesting that the New Zealand flies are derived from North American populations. In the late 1980s, D. pseudoobscura was found at multiple sites in New Zealand (Moore and Chambers 1991). We have collected numerous D. pseudoobscura from two sites in New Zealand.
In this study we genotyped D. pseudoobscura captured from populations in New Zealand and North America at 10 variable microsatellites (Noor et al. 2000b). Heterozygosity, allele frequencies, and loss of alleles were compared between populations for these loci. We document a founder event in the movement of D. pseudoobscura from North America to New Zealand and estimate its severity.
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Materials and Methods |
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Fly Stocks and DNA Preparation
Wild-caught male and female D. pseudoobscura were used for this study. North American D. pseudoobscura were collected in Mt. Ellen, Utah, and Tempe, Arizona. New Zealand D. pseudoobscura were collected in Christchurch and Lincoln, New Zealand. Fly DNA was extracted from single-fly squish preparations (Gloor and Engels 1992).
Microsatellite Analysis
All microsatellites used in this study were described previously (Noor et al. 2000b; see also Table 1). For microsatellite assays, one primer was ordered with an M13 tail at the 5' end, and polymerase chain reaction (PCR) was performed in a 10 µl reaction volume with 0.5 pmol of each primer, 0.4 pmol fluorescent dye labeled M13, 200 µM dNTPs, 1 µl 10x buffer (100 mM Tris pH 8.3, 500 mM KCl, 15 mM MgCl2), 1 U Taq polymerase, and 1 µl from a 50 µl single-fly squish preparation. PCR was executed using a touchdown cycle (Palumbi 1996). Following PCR, 3 µl of LiCor stopping buffer was added to the reactions and 1 µl was loaded onto an acrylamide gel (National Diagnostics, Atlanta, GA) on a LiCor 4200 DNA analyzer for visualization. Allele sizes were calculated using RFLPscan (Scanalytics, Inc., Fairfax, VA) by comparison to LiCor DNA size standards.
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Data Analysis and Computer Simulations
The measure of genetic differentiation, FST, was calculated between Christchurch and Lincoln in New Zealand and between Arizona and Utah in North America using FSTAT (Goudet 1995). Populations within North America and within New Zealand were not significantly differentiated (FST not significantly different from zero for both; see Results); therefore, the data within each geographical area/continent were pooled. Differences in allele frequency were estimated as one minus the proportion of shared alleles (1 - Psa) (Bowcock et al. 1994; Noor et al. 2000a). Expected heterozygosity was calculated as H = (n/[n - 1])(1 -
pi2), where n is the number of alleles scored and pi is the frequency of the ith allele. To test for recent bottlenecks through heterozygosity excess, data from New Zealand and North America were analyzed with the program BOTTLENECK (Cornuet and Luikart 1996; Piry et al. 1999). Data were analyzed using both the infinite alleles model and the stepwise mutation model. MULTSIM was previously used to study the spread of D. subobscura in North America (Noor et al. 2000a). MULTSIM was modified to evaluate founder events using heterozygosity and allelic loss in addition to allelic frequency changes. Input into MULTSIM are the allele frequencies in the ancestral population and a measure of differentiation between ancestral and founder populations (e.g., 1 - Psa). MULTSIM then randomly samples various numbers of alleles to "found" a hypothetical new population, and evaluates the probability of observing equal or greater genetic differentiation to that noted between ancestral and founder populations with the number of alleles sampled. For example, if 10,000 alleles are sampled, then very little differentiation is expected between ancestral and founder populations, whereas if only 10 alleles are sampled, then extensive differentiation is expected. MULTSIM uses haploid founder numbers, which would be roughly equivalent to the number of founding chromosomes, and hence should be interpreted differently for X-linked versus autosomal microsatellites. The recovery of the founding population was simulated as an instantaneous increase to a population of sufficient size to minimize the effect of genetic drift (>5000) (Noor et al. 2000a) or stepwise recovery with each generation increasing in haploid number by a factor of two.
The program went through 1,000 iterations and evaluated the percentage of simulations in which the observed New Zealand population had allelic loss, heterozygosity changes, or 1 - Psa that seemed consistent with the observed data. Minimum and maximum numbers of founders could be estimated based on conditions in which 95% of the simulated results were consistent with the observed results. We also combined the data from the loci on the X chromosome separately from the estimates for the autosomes to obtain ranges of probable founder numbers. To do this we multiplied the probabilities for the observed parameter (1 - Psa, heterozygosity, allelic loss) for the five loci on the X chromosome or the five loci on the autosomes (Edwards 1992). The combined range of founder numbers reported for each parameter is where 95% of the simulations are above the lower limit and 95% of the simulations are below the upper limit. The approximate number of founding individuals can be estimated by dividing the number of haploid founders by four for loci on autosomes and three for loci on the X chromosome (Noor et al. 2000a).
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Results |
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Populations Within a Geographic Area Can Be Considered One Population
D. pseudoobscura from two sites in North America and two sites in New Zealand were variable at all loci examined: five microsatellite loci on the X chromosome and five microsatellites on the autosomes. Calculations of FST suggested that populations within North America and within New Zealand have no significant genetic structure (Table 2), and the data within each of the two continents was pooled for subsequent analysis. Previous studies have also found minimal differentiation among North American D. pseudoobscura populations (Noor et al. 2000b). We observed a statistically significant structure between North America and New Zealand (FST = 0.120, P <.001), consistent with the occurrence of a strong genetic bottleneck.
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Genetic Parameters Indicate a Bottleneck Resulting from the Spread of North American D. pseudoobscura to New Zealand
Three genetic parameters-heterozygosity, allele loss, and change in allelic frequency (measured as 1 - Psa)-were estimated from the frequency data of alleles at 10 independent microsatellite loci. Expected heterozygosity (used throughout the article) ranged from 0.284 to 0.922 for North America and 0.392 to 0.807 for New Zealand (Table 2). As expected for a founding event, the heterozygosity is lower at eight loci in New Zealand compared to North America. It is not surprising that all loci do not show a reduction in heterozygosity, as heterozygosity is often considered to be a weak indicator of a founding event (Allendorf 1986; Luikart et al. 1998b).
All loci lost at least one allele in the spread from North America to New Zealand (Figure 1). Allelic loss was especially pronounced in X-linked microsatellites, in which a minimum of 50% of the alleles were lost at each locus. The New Zealand population has alleles at two autosomal loci (gld and mlc) that were not observed in the North American population. It is possible that these alleles are rare in the North America population, and the founder effect may have caused them to be disproportionately represented in the New Zealand population. Assuming these are not new mutations, these unique alleles were probably present at a frequency of less than 5% in the North American populations we sampled, as a minimum of 117 haploid samples were analyzed for each locus, indicating that we had a 95% chance of detecting alleles with a frequency greater than 0.025 and a 99.75% chance of detecting alleles with a frequency greater than 0.05.
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Allelic frequency also changed from North America to New Zealand as indicated by the measure 1 - Psa (Table 2) (Bowcock et al. 1994). X-linked loci were more strongly differentiated between continents than autosomal loci, as reflected by 1 - Psa: 0.598 for X-linked loci and 0.244 for loci on the autosomal chromosomes (P <.0015, Student's t-test). All three estimates of genetic parameters indicate that the New Zealand D. pseudoobscura population has less genetic diversity than the North American D. pseudoobscura population, as expected following a founding event.
We analyzed the allele frequencies using the program BOTTLENECK (Cornuet and Luikart 1996; Piry et al. 1999), which computes for each population sample and locus the distribution of the expected heterozygosity and compares it to the observed heterozygosity under the assumption of mutation-drift equilibrium. Three separate statistical tests are performed using the program BOTTLENECK to assess whether the New Zealand population fits the criterion for a recent bottleneck (Cornuet and Luikart 1996; Luikart et al. 1999). BOTTLENECK did not detect significant evidence of a recent bottleneck (excess of heterozygosity) under either a stepwise mutation model (P >.11) or an infinite alleles model (P >.06). As BOTTLENECK only detects recent founding events, this observation suggests that the founding event occurred more than 40 generations ago (0.25–2.5 times 2Ne) (Cornuet and Luikart 1996). This is consistent with the historical data on the colonization of this species.
At Least Six Founding Individuals Are Required
Using the number of alleles identified in the founded population, it is possible to ascertain a minimum number of founders. Because the runt locus has at least 10 alleles, a minimum of 10 haploid founders were required for founding the population, assuming no new mutations in the runt locus. This is a reasonable assumption given the recent colonization (approximately 50 years ago) of the New Zealand population. The runt locus is on the X chromosome, so the minimum of 10 haploid founders is equivalent to at least six founding individuals (e.g., five females and one male are required).
Founder Numbers Estimated from Genetic Parameters
Computer simulations using MULTSIM (Noor et al. 2000a) evaluated possible initial founder numbers based on the genetic data obtained from New Zealand and North American D. pseudoobscura. We ran our simulations estimating a twofold increase in population size per generation (Table 3). To evaluate possible effects from rare alleles in North America that were not sampled, we also pooled all alleles present at less than 5% in the founder population and reanalyzed the data. Only very minor differences were seen in the range of potential founder numbers (data not shown), indicating that rare alleles potentially missed by our sampling would not dramatically affect our analyses.
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The haploid founder number estimates were consistently narrower when derived from loci on the X chromosome (2–70, all loci combined) than loci on the autosomes (2–200, all loci combined). Different genetic parameters gave different estimates of the severity of the founding event, particularly the upper limit for the range of founder numbers. For example, simulations using allelic loss yielded higher estimates of the range of founder numbers than simulations using the other parameters. Overall, the range of founder numbers varied greatly, though almost all calculations indicate fewer than 140 haploid founders (excludes allelic loss for gld, which did not resolve for the upper limit). Using the allelic loss data, we calculated the most likely number of founders based on loci on the X chromosomes or the autosomes separately. To do this we multiplied the probability that each founder number would give rise to the observed data across all loci. The highest combined probability would indicate an estimate of founder number. This approach estimated 13 haploid founders when considering the loci on the X chromosomes and 45 haploid founders using loci on the autosomes.
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Discussion |
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D. pseudoobscura was identified in New Zealand earlier this century. We have demonstrated that the New Zealand population of D. pseudoobscura has substantially less genetic diversity than the ancestral North American population, consistent with the founding of the New Zealand population by a small number of individuals. All 10 microsatellite loci examined had fewer alleles in the New Zealand population than in the North American population and 8 of 10 loci had lower expected heterozygosity in the New Zealand population. FST between North America and New Zealand is large and statistically significant (0.12 ± 0.03). D. pseudoobscura appear to have migrated from North America to New Zealand and suffered a severe founder event.
The founder event had a more pronounced effect on X-chromosomal microsatellites than autosomal microsatellites. One factor that may contribute to this effect is the potentially different contributions from loci on X chromosomes and autosomes to founder populations: three alleles for X chromosomes and four alleles for autosomes, assuming an equal number of males and females and singly mated females only. Even taking this into account, the founder effect is much more pronounced for the X-linked loci than those on the autosomes for all parameters examined: allelic loss, change in allele frequencies, and loss of heterozygosity. If multiple males mated with each founding female, this difference between X and autosomal founder effects may be expected. This could suggest a sex-ratio bias toward males among the founders or selection following the founder event acting preferentially on linked loci on the X-chromosome (e.g., Charlesworth et al. 1987).
Bottleneck and founder events have different characteristics immediately after the event than are observed after many generations. There will be a heterozygosity excess immediately after the bottleneck because the allelic diversity is reduced faster than heterozygosity (Cornuet and Luikart 1996; Nei et al. 1975). Additionally, the range of allelic frequencies will change in a characteristic manner immediately after the bottleneck, and this shift in allelic frequencies is transient and will revert to the expected frequency ranges in subsequent generations (Luikart et al. 1998a). Therefore both heterozygosity and allelic frequency can be used to detect early bottlenecks and founder events (Cornuet and Luikart 1996). We were unable to detect evidence of a founder effect in D. pseudoobscura from New Zealand using these characteristic differences, as evaluated in the computer program BOTTLENECK (Cornuet and Luikart 1996; Piry et al. 1999) or by Luikart's graphical method (Luikart et al. 1998a). This suggests that sufficient time has passed since the founder event for the early indicators to return to expected values. These methods are unable to evaluate founder events that have recovered from the initial disruption of heterozygosity and allelic frequency. The method described herein is useful for evaluating founding events that are sufficiently far back to have recovered from the initial distortions in allelic frequency, but are too recent to have significant accumulations of mutations which can be used in analysis.
Although founder events are often readily detected, and some estimate of the severity can be determined from genetic data, it is generally difficult to know the details surrounding the founding event, such as time of founding and founder number. Only in a limited number of cases are historical data available to establish the severity of the bottlenecks or founding events (e.g., Glenn et al. 1999; Leberg 1992). Most estimates of founder number rely on new mutations (e.g., LePage et al. 2000; Rogers and Harpending 1992; Storz and Beaumont 2002). However, methods utilizing mutation rates are not useful for studying very recent bottlenecks or founder events, as there has not been sufficient time for the accumulation of mutations. In addition to our standard analyses, we utilized a previously developed method that relies exclusively on changes in allele frequencies, allele numbers, and heterozygosity to evaluate possible numbers of founders (Noor et al. 2000a). This approach does not rely on knowing mutation rates or having equilibrium conditions within the source or founder populations. We assume a rate of increase and loose agreement with haploid inheritance. The latter assumption would be violated by strong sexual selection in the founder population. However, empirical data have generally supported weaker sexual selection in recently founded populations rather than strong sexual selection (Kaneshiro 1989). Our approach is similar to a method recently described by Launey et al. (2001), which estimates the effective number of breeders in a population immediately after a bottleneck. The allelic loss in bottlenecks of various intensity are modeled based on the known allelic composition before the bottleneck. Results of hypothetical bottlenecks are compared to the experimentally known allelic loss to obtain 95% confidence intervals for the founder numbers. The results of this approach corroborated our hypotheses based on the raw data that the initial founding in New Zealand by D. pseudoobscura was probably by a very small number of individuals.
The analysis of founder effects has great potential to aid in conservation efforts as well as studying the evolutionary process. For the colonization of D. pseudoobscura in New Zealand, allelic loss and allelic frequency proved to be more robust methods for determining the severity of the founding event. The methodology used in this article complements other methods for analysis of recent bottlenecks (Cornuet and Luikart 1996) and more ancient bottlenecks (Rogers and Harpending 1992). This procedure could be extended to species of greater conservation interest.
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Acknowledgments |
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We thank J. C. Larkin and D. Ortíz-Barrientos for helpful comments on the manuscript. Funding was provided by National Science Foundation grant 9980797 (to M.A.F.N.) and National Institutes of Health grant GM58060 (subcontracted through J. Hey at Rutgers University to M.A.F.N.).
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Footnotes |
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Corresponding Editor: R. C. Woodruff
Received May 11, 2002
Accepted September 30, 2002
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