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Gene Flow by Pollen Into Small Populations

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Gene Flow by Pollen Into Small Populations Proc. Natl. Acad. Sci. USA Vol. 86, pp. 9044-9047, November 1989 Population Biology Gene flow by pollen into small populations: Data from experimental and natural stands of wild radish (Raphanus sativus/spatial isolation/interpopulation mating) NORMAN C. ELLSTRANDt, B. DEVLINt, AND DIANE L. MARSHALL§ Department of Botany and Plant Sciences and Program in Genetics, University of California, Riverside, CA 92521-0124 Communicated by R. W. Allard, August 14, 1989 (received for review August 18, 1988) ABSTRACT Gene flow can have an especially strong im- much from population to population, whether it varies within pact on the evolution of small populations. However, empirical a population over a season, and whether it varies with spatial studies on the actual rates and patterns of gene flow into small isolation from the nearest conspecific. More data are needed populations are few. Thus, we sought to measure gene flow into that focus more closely on a number ofpopulations ofa single small populations of wild radish, Raphanus sativus. We found species. significant differences in gene flow receipt among experimental Therefore, we selected wild radish, Raphanus sativus L. populations and within those populations over a season. A (Brassicaceae), to measure patterns of gene flow by pollen maximum-likelihood estimate revealed that almost all of the into small populations. This species is especially suitable for gene flow into these synthetic populations had its origin in both experimental and descriptive gene flow studies because relatively distant (>650 m), large natural populations rather it is a common outcrossing weed in southern California (8), than the proximal (255400 m), small synthetic populations. is easy to grow and transplant (9), is polymorphic for several We also estimated rates of interpopulation mating from simple isozyme loci that are expressed in both adult and seedling paternity analysis of progeny produced by seven small (ca. 50 tissues (10), and has been the subject of prior gene flow study plants) natural populations. Again, we found significant het- (11, 12). First, we used three small, genetically structured, erogeneity in gene flow receipt. Although these populations synthetic populations to measure interpopulation mating varied 10-fold in their range of isolation distances (100-1000 rates and to measure the gene flow coming into these popu- m), gene flow rates did not vary with distance. The magnitude lations from more distant, large natural populations. We of gene flow rates estimated in all but one population was great sampled from these populations periodically to ask whether enough for gene flow to play an important role in the evolution gene flow varies over time within a season. Second, we of these small populations. measured gene flow received by seven small natural popu- lations and asked whether the rates measured varied with the Gene flow has considerable potential as an evolutionary populations' spatial isolation. In both studies, we could not force. Theory indicates that even a moderate rate of gene find any simple relationship of gene flow by pollen to dis- flow is sufficient to counteract the diversifying effects of tance, implying that, for the spatial scale studied, factors local, directional selection, or genetic drift (1). Gene flow can other than distance are more important in determining this have an especially strong impact on the evolution of small critical evolutionary force. populations. Immigration of a few individuals will counteract selection more readily in a small population than a large one MATERIALS AND METHODS (2). Furthermore, although drift becomes more important in smaller populations, a single immigrant per generation will Studies of Synthetic Populations. In February 1987, we suffice to prevent drift (3). created three experimental, genetically structured popula- Not only is gene flow important to the microevolutionary tions of wild radish at the Moreno Valley Field Station of the dynamics of small populations, but such populations are also University of California at Riverside. Natural populations of thought to be especially vulnerable to gene flow by pollen wild radishes occurred at every edge of the Field Station, but because of decreased opportunities for short-range mating were >650 m from each of the experimental populations. To and increased opportunities for receiving the fixed amount of obtain our experimental plants, we electrophoretically pollen arriving from outside the population (4). For example, screened seedlings derived from seed collected at the Field experiments with crop plants have demonstrated that the rate Station in 1986. The seedlings were screened at the following ofgene flow by pollen from source plants bearing a dominant loci: triose phosphate isomerase (TPI), acid phosphatase marker increases as the size of the recipient population (ACP), and two phosphoglucomutase loci (PGMI and decreases (reviewed in ref. 4). Much less is known of rates of PGM2). We obtained allele frequencies of the pollen pool of gene flow into small populations ofnatural species. A handful nearby natural populations from a sample of 320 plants. of studies have used paternity analysis and related methods Details of the electrophoretic procedures have been reported to estimate the rate of gene flow by pollen into small (10). populations (reviewed in ref. 5). These studies reported All experimental individuals were chosen to be monomor- considerable variation in the amount of gene flow detected, phic at the TPI and ACP loci for the same allele. The from as low as 0.1% in Picea glauca (6) to as high as 88% in frequencies of these alleles in the surrounding natural pop- Pinus elliottii (7). However, since almost all of these studies ulations were 0.951 for the TPI allele and 0.824 for the ACP reported on only one or two populations, they provide little allele. These loci are not linked (10). insight into typical patterns of gene flow into small popula- tions for these species, such as whether gene flow varies tTo whom reprint requests should be addressed. tPresent address: Division of Biostatistics, Laboratory of Epidemi- ology and Public Health, Yale University, P.O. Box 3333, New The publication costs of this article were defrayed in part by page charge Haven, CT 06510. payment. This article must therefore be hereby marked "advertisement" §Present address: Department of Biology, University of New Mex- in accordance with 18 U.S.C. §1734 solely to indicate this fact. ico, Albuquerque, NM 87131. 9044 Downloaded by guest on September 30, 2021 Population Biology: Ellstrand et A Proc. Natl. Acad. Sci. USA 86 (1989) 9045 The plants making up the experimental populations were likelihood estimate of Y, the number of cryptic long-distance chosen so that the paternal contributions of each population matings. could be distinguished from those of the remaining popula- Furthermore, because pollen gametes from the natural tions. To attain this goal, each population was genetically populations can carry the same alleles at PGMI and PGM2 structured with different PGMI and PGM2 genotypes. Plants as the synthetic populations, such gametes might mimic gene making up population 1 had PGMI genotypes of22, 23, or 33 flow among the planted populations. Consequently, before with a PGM2 genotype of 33; those making up population 2 examining gene flow among the synthetic populations per se, had PGMI genotypes of 00, 01, or 11 with PGM2 genotypes a second analysis must be performed to estimate how many of 11, 12, 22, 13, 23, or 33; and those making up population pollen gametes from the natural populations would be mis- 3 had PGMI genotypes of22, 23, or 33 with PGM2 genotypes assigned as arising in alternate synthetic populations. 11, 12, or 22. In matings among these populations, paternal To illustrate our approach, consider population 1. This contributions from population 2 could be distinguished by a population had only PGMI alleles 2 and 3 and PGM2 allele progeny's PGMI genotype; the others are distinguished by 3. Gene flow from the other synthetic populations is detect- their PGM2 genotype. The PGMI allele frequencies of these able from progeny bearing PGMI alleles 0 or I or from loci in the natural populations were 0.211, 0.239, 0.385, and progeny bearing PGM2 alleles I or 2. Applying simple 0.165 for alleles 0, 1, 2, and 3, respectively; for PGM2, 0.220, probability rules, the number of undetected gametes from 0.392, and 0.388, respectively, for alleles 1, 2, and 3. These natural populations that mimic gene flow from populations 2 loci are also not linked (10). or 3 is given by: We transplanted the seedlings at the rosette stage. The three populations were planted in a triangular pattern, iso- T = (0) * [p(I) + p(2) - p(1) * p(2)] * (X + Y) lated from each other at distances of255, 280, and 400 m, with populations 2 and 3 the most distant and populations 1 and 3 where p(J) is the probability that a gamete from the natural the least distant. Each population consisted of 15 plants populations has allele 2 or 3 at PGMI and p(2) is the arranged in a 3 x 5 pattern with 2-m spacing. probability that a gamete from the natural populations has Flowers were naturally pollinated. Floral visitors (pre- allele 3 at PGM2. (The value of the expression within sumed pollinators) were mainly syrphid flies early in the brackets is the probability that the natural populations pro- season; numbers of honeybees and lepidoptera increased duce a gamete that would mimic gene flow from populations with the season as did the overall visitation rate. To test for 2 or 3.) temporal heterogeneity in gene flow, flowering stems on each Studies of Natural Populations. From 1982 to 1986, we used plant were labeled once a week. Fruits were harvested when paternity exclusion analysis to measure rates of apparent mature. About 150 to 200 seeds from each population were gene flow (11) for seven small, natural wild radish popula- collected from fruits fertilized during the weeks of April 11, tions in Moreno Valley and Riverside.
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