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Homozygosity and Patch Structure in Plant Populations As a Result of Nearest-Neighbor Pollination (Inbreeding/Population Structure/Isolation by Distance) MONTE E

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Homozygosity and Patch Structure in Plant Populations As a Result of Nearest-Neighbor Pollination (Inbreeding/Population Structure/Isolation by Distance) MONTE E Proc. Nati Acad. Sci. USA Vol. 79, pp. 203-207, January 1982 Population Biology Homozygosity and patch structure in plant populations as a result of nearest-neighbor pollination (inbreeding/population structure/isolation by distance) MONTE E. TURNER, J. CLAIBORNE STEPHENS, AND WYATT W. ANDERSON Department of Molecular and Population Genetics, University of Georgia, Athens, Georgia 30602 Communicated by G. Ledyard Stebbins, August 24, 1981 ABSTRACT The population genetic consequences of nearest- ported sufficiently often for other plants and pollinators (5-15) neighbor pollination in an outcrossing plant species were investi- that it is clearly an important characteristic of pollination biol- gated through computer simulations. The genetic system consisted ogy. It is not universal, however, and there is at least one case of two alleles at a single locus in a self-incompatible plant that (7) in which one pollinator serving a plant species shows NNP, mates by random pollen transfer from a neighboring individual. while others do not. Several workers (6-10) have noted that Beginning with a random distribution ofgenotypes, restricted pol- predominantly NNP should restrict gene dispersal in plant pop- len and seed dispersal were applied each generation to 10,000 in- ulations. Schaal (11) reported extensive local differentiation for dividuals spaced uniformly on a square grid. This restricted gene 15 polymorphic loci coding for soluble enzymes in a population flow caused inbreeding, a rapid increase in homozygosity, and ofthe herb Liatris cylindracea. She found highly significant in- striking microgeographic differentiation ofthe populations. Patches creases in homozygosity within neighborhood-sized quadrats of homozygotes bordered by heterozygotes formed quickly and persisted for many generations. Thus, high levels of inbreeding, and significant differences between quadrats. homozygosity, and patchiness in the spatial distribution of geno- Although the effects of NNP on restricting gene dispersal in types are expected in plant populations with breeding systems plant populations have been discussed for many years, there based on nearest-neighbor pollination, and such observations re- appears to be no quantitative analysis of this specific case of quire no explanation by natural selection or other deterministic restricted gene flow, and information on several points such as forces. the number, size, and persistence of genotypic patches is not provided by more general studies ofbreeding systems. The the- over the habitats they ory of Wright (1) and the simulations of Rohlf and Schnell (4) Genetic differentiation of populations may not reflect the biological situation ofNNP. Hence we have occupy is a major factor in the processes ofadaptation and evo- undertaken computer simulations to study the manner in which lution. For populations subdivided into small colonies, it is easy of to picture this differentiation as the result of genetic drift. homozygosity, population structure, and spatial patterns ge- Wright (1-3) showed that even large populations distributed notypes develop in plant populations in which breeding occurs continuously over an area will differentiate if gene dispersal mostly by NNP. In particular, our model allows seed dispersal. within them is sufficiently restricted. He termed this process Additionally, we have not allowed any self-fertilization, because isolation by distance. Many genetic characteristics of such con- the increased inbreeding and patchiness due to selfing is well tinuous populations depend on the size oflocal breeding units, known. We have attempted in this way to make our simulations or neighborhoods, within them. In particular, the smaller the more conservative than other models (1, 4). neighborhoods, the greater the genetic differentiation in the THE MODEL population, so these neighborhoods are essentially subdivisions created by limited gene dispersal. Inbreeding and increased We wrote a computer program to simulate the population ge- homozygosity result, as does a spatial differentiation ofgene and netics of an annual plant species visited by pollinators whose genotype frequencies. The genetic structure of a population flights are predominantly between nearest neighbors. Two al- departs considerably from that expected in a random-mating leles at a single locus composed the genetic system. The pop- population. Rohlf and Schnell (4), using computer simulations ulation of self-incompatible, bisexual diploid plants was uni- of Wright's model to examine spatial patterning and genetic formly distributed on the intersection points ofa 100 x 100 grid. differentiation in populations with various neighborhood sizes, Flowering and reproduction of all individuals in the population observed rapid establishment of spatial patterns in gene fre- were synchronized, so the generations were nonoverlapping, quency, which persisted for many generations. and population size remained a constant 10,000. Our simulation Many plant species have reproductive systems ideally suited was similar in basic design to that of Rohlf and Schnell (4), al- to isolation by distance. Pollinator flight behavior and seed dis- though our model was structured to fit the particular biological persal determine gene flow, and both are often severely lim- situation of NNP. Our assumptions about selfing, seed disper- ited. The restriction on pollen movement is particularly strong sal, and mate selection were somewhat different than theirs, when pollinators fly between nearest-neighboring plants, a and our spatial analysis was based on the distribution of geno- common behavior. Levin and Kerster (5), for example, observed types rather than gene frequencies. A simplified flow chart of almost exclusively nearest-neighbor pollination (NNP) in Liatris the computer program is presented in Fig. 1. aspera (Compositae), as well as highly localized dispersal of A male parent is selected from plants neighboring the female seeds. Even with some carryover ofpollen from previous visits, parent in one ofthe two ways diagrammed in Fig. 2. With strict gene dispersal was highly leptokurtic (6). NNP has been re- NNP the four nearest plants on the grid have equal probabilities (P = 0.25) of serving as male parent. With relaxed NNP the 12 of The publication costs ofthis article were defrayed in part by page charge nearest neighbors of the female parent have probabilities payment. This article must therefore be hereby marked "advertise- ment" in accordance with 18 U. S. C. §1734 solely to indicate this fact. Abbreviations: NNP, nearest-neighbor pollination. 203 Downloaded by guest on September 30, 2021 204 Population Biology: Turner et al. Proc. Nad Acad. Sci. USA 79 (1982) 1 Initiate Population in 2 Hardy-Weinberg Proportions Calculate F and and Randomly Place Other Parameters on a 100x1OO Grid I 5 Randomly Choose .4 Randomly Select 3 Go to Plant at a Gamete from 4- Parent from Nearest First Position on Grid Each Parent Neighbors of Parent and Use as g Parent ? L I I 8 6 7 Combine df and g NO 8 Go to Plant at Next Gametes to Form an Have All Plants Been Position on Grid and Offspring Genotype Used as ? Parent? Use as g Parent YES 10 9 Replace Each Plant NO Have All Generations A with the Offspring Been Completed? Formed in Box #6 YES 11 L--p STOP FIG. 1. Simplified flow chart of the computer program used to simulate plant populations breeding under NNP. serving as male parent according to their distance from the fe- RESULTS AND DISCUSSION male parent. There are two ways this latter case can be inter- preted biologically. Pollinators can move to plants which are Inbreeding and Homozygosity. The inbreeding effect of first, second, and third nearest to the maternal parent with the NNP was measured by the coefficient of inbreeding, F. We probabilities given. Alternatively, pollinators could move to calculated F as simply the proportional loss of heterozygosity nearest-neighboring plants only, carrying mostly pollen from from Hardy-Weinberg expectation: F = (expected heterozy- the last plant visited, but in addition some pollen from earlier gosity - observed heterozygosity)/expected heterozygosity. In visits to other plants. The plant visited next to last contributes this paper the values of F reported are exact, because all indi- most of this carryover pollen, with rapidly declining contribu- viduals in our simulated populations were censused. tions from successively earlier visits. The results of our simulations are summarized as values of Each individual has a probability of0.8 ofbeing replaced by F in Fig. 3. Simulations with the same parameters but different its own maternally derived seed. Seed dispersal was incorpo- sequences of pseudorandom numbers gave strikingly similar rated by allowing a probability of 0.2 that an individual would results. In all cases the variability of F among the 10 replicate be replaced by a seed formed from a neighboring (strict NNP, populations was quite small, with standard deviations less than Fig. 2 Left) individual. Computer runs were made with three 0.03. choices ofgene frequencies: P = 0.5, P = 0.8, and P = 0.9, each It seems that the gene frequency has little effect on either with both strict and relaxed NNP (Fig. 2). Ten replicate pop- the trajectory or the final value ofF (Fig. 3B). Thus we feel jus- ulations were simulated for each choice of gene frequency and tified in comparing our results to studies, such as that of Schaal neighborhood size, each utilizing a different sequence of pseu- (11), which present F values averaged
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