INBREEDING/SELFING/OUTCROSSING

Transcription

1 INBREEDING/SELFING/OUTCROSSING A. THE QUESTIONS. Is the trait vulnerable to inbreeding depression? What is the selfing or outcrossing rate in the population? How many mating partners are represented in the progeny of an individual? B. BASIC IDEAS. Our focus is on the mating systems of natural populations of plants and animals. By the mating system we mean a population characterization based on the numbers and relatedness of mating partners. In the case of plant mating systems in which a certain proportion of offspring are produced by selfing each generation (partial selfing), the key issues are the degree of selfing and the consequences of that selfing (inbreeding). In the case of small populations of plants and animals, the issue is the consequences of inbreeding. In the case of outbred animal populations, the key issues are the number of mating partners and the relationship between that number and fecundity. 1. Inbreeding (Lynch & Walsh 1998, chap 10; Falconer & Mackay 1996, chaps ; Wright 1977, chaps. 1-2). a. For fitness and fitness related traits, dominance at individual loci is often in the direction of increased values of a trait. This empirical result is probably a consequence of persistent directional selection on such traits. b. Homozygosity incurred by inbreeding causes the mean of the trait to shift downward. 2. Number of mating partners (Arnold & Duvall 1994, Arnold 1994b). a. The number of mating partners that bear progeny is a natural currency for measuring sexual selection. b. Sexual selection (Bateman) gradients are based on that currency and provide a characterization of the mating systems that can be related to evolutionary theory. C. EARLY EMPIRICAL WORK ON INBREEDING. 1. Darwin's (1876, 1882) perspective on inbreeding ("Nature... abhors perpetual selffertilization"). Darwin paid much attention to breeding systems in plants and was aware of the deleterious consequences of inbreeding. He interpreted many features of flower morphology and phenology as adaptations to prevent selfing (e.g., heterostyly) and hence inbreeding. 2. Differentiation of livestock breeds ("the best of the best, the worst of the worst"). The differentiation of livestock breeds is a consequence of both selection and inbreeding. In an effort to perpetuate favored characteristics in a selected line, the animal breeder may intentionally or unintentionally institute a program of inbreeding. Selection promulgates the best of the best, but inbreeding often perpetuates the worst of the worst. 3. Wright's guinea pig lines (Wright 1977, Slides 1 & 2). Sewall Wright s first job as a recent PhD was to analyze and continue a study of inbreeding in guinea pigs for the US Dept. of Agriculture. The experience forced Wright to concentrate on the problems of small population size and led to the modern, population genetic theory of inbreeding. D. THEORY OF INBREEDING (Crow & Kimura 1970, chap. 3). The model of phenotypic value includes dominance and epistatic effects, as well as additive effects, to capture the essential, empirically-established features of inbreeding. 1. Identity by descent (Cotterman 1940, Malécot 1948). The crucial parameter in understanding inbreeding was independently discovered by Cotterman in the USA and Malécot in France, viz., identity by descent (ibd).

2 2. Inbreeding coefficient, f = the probability that two alleles at a locus are identical by descent. As both Cotterman and Malécot realized, we wish to know not just the probability that two alleles at a locus are homozygous, we wish to know the probability that both are inherited from the same ancestor. The idea is that if a deleterious allele exists in an ancestor, two copies of that allele (identical by descent) may reach the genome of a descendant. Because two copies reach the descendant, those deleterious recessive alleles will be expressed. a. Pedigrees and the gene drop analogy. No matter how complicated an individual s pedigree, we can calculate the probability that two alleles at a locus in that individual are ibd. The calculation of this probability can be visualized as a simulation in which a colored ball that is repeatedly dropped down through the pedigree, so that two copies of the colored ball end up in the target individual s genome. The simulation gives a estimate of the inbreeding coefficient. Of course, the simulation is unnecesary because f can be calculated directly. b. Uses in plant and animal breeding and in captive propagation. In the captive propagation of rare and endangered species, pedigrees or stud books are maintained so that the best choice of mating partners can be made each generation. A primary consideration in those choices is minimizing the inbreeding coefficient of the resulting progeny. 3. Effects of inbreeding from an outbred base population (Crow & Kimura 1970, chap. 3; Falconer & Mackay 1996, chaps ; Slides 3-4). Genetic models can be used to predict the population-level consequences of continued inbreeding, starting with an outbred base population. There are three main consequences: a. Decrease in heterozygosity. b. Decline in the means of quantitative traits (inbreeding depression). c. Decrease in variance within lines, an increase in variance among lines, and an increase total variance. 4. Causes of inbreeding depression (Charlesworth & Charlesworth 1987, Lynch 1991). Partial dominance and overdominance are two alternative theories for the basis of inbreeding depression. a. Partial dominance (favorable alleles tend to be dominant or partially dominant; alternatively, deleterious alleles tend to be recessive). b. Overdominance (phenotypic value of heterozygote greater than either homozygote). E. SURVEY OF ISSUES AND METHODS 1. Measurement of inbreeding depression (Lynch & Walsh 1998, chap. 10). a. Single-generation analysis.- Compares mean phenotypes of offspring from randomly bred parents with offspring from matings between close relatives (Slides 5-6). b. Multi-generation analysis.- Tracks mean phenotype as a function of inbreeding coefficient. The resulting data are often analyzed by compute regression of phenotypic mean on inbreeding coefficient. Linear and curvilinear regressions can be compared to test for curvilinearity, an indication of epistasis (Slides 7-8). c. Ritland s method (uses molecular markers to estimate selfing rate and inbreeding coefficients in natural populations with partial selfing). 2. The importance of inbreeding depression in populations with partial selfing (Charlesworth & Charlesworth 1987) a. Inbreeding depression as a measure of the cost of self-fertilization (Slides 9-11). Inbreeding depression in fitness components or fitness-related traits is a focus in assessing these costs. One measures the fitness of progeny produced by selfing and by outcrossing. The difference in mean fitness (outcrossed selfed) provides

3 an estimate of inbreeding depression. b. Measuring the outcrossing rate. Inbreeding depression measures of the cost of selfing given that selfing has occurred. Another key parameter of interest is the probability that selfing occurs, or - alternatively the outcrossing rate. The selfing rate can be estimated in two ways: i. Using inbreeding depression (D. Charlesworth). ii. With molecular markers (Shaw & Allard 1982; Weir 1990, chap.8; Ritland 1990a,b). 3. Systematic inbreeding as a tool (see also Falconer & Mackay, chap. 16). a. The uses and limitations of inbred lines. Inbred lines can be used to isolate and map the genes genes that affect a phenotypic character (Chapter 13). Inbreeding depression can arise in such a line, and the resulting decline in fitness can cause the line to be lost. Consequently, any study based on a set of lines derived by inbreding must assess the consequences of bias introduced by line extinction. b. Detecting polygenic mutation (Lynch 1988a). Deliberate selection on lines derived by inbreeding can be used to estimate the contribution of mutation to genetic variance. 4. Measuring inbreeding on a pedigree (Crow & Kimura 1970). Given a pedigree, one can determine the inbreeding coefficient of any individual: past, present and future. Such calculations a key aspect of captive or controlled propagation of small populations. 5. Characterization of the mating system (Bateman 1948; Arnold 1994a, 1994b; Arnold & Duvall 1994; Slides 12-14). In many plant and animal populations, the number of mating partners is the issue rather than selfing rate. The number of mating partners and its relationship to fecundity has a direct relationship to the potential for sexual selection in the population. a. Multiple paternity assessment (Meagher 1986; Williams & Evarts 1989; Weir 1996, chap. 8). Neutral, molecular markers can be used to determine or estimate the parentage of individuals in a natural population. A variety of programs are available online to analyze these kinds of data: e.g., Cervus and Gerud b. The parental table and the measurement of Bateman gradients (Arnold & Duvall 1994). see excel spreadsheet. Bateman gradients can be used to compare the intensity of sexual selection acting on males and females and hence to characterize the mating system. To compute these gradients, the data from a parentage analysis are organized in a parental table. The parental table has male and female names as row and column labels. Each cell in the table has a entry denoting the number of progeny produced by a particular male and female. From such a table one can compute the number of mating partners for each male and female, as well as their total fecundities (number of progeny). Using those numbers, one can plot the male fecundity as a function of number of mating partners, as well as female fecundity as a function of number of mating partners (Slide 12). The regressions fitted to those data (Slide 13), called Bateman or sexual selection gradients, estimate the final common path from trait to fitness that arises due to sexual selection (Slide 14). The variance in mating success of males and females (Slide 12) can be used to place an upper bound on the intensity of sexual selection. F. DESIGN OF INBREEDING EXPERIMENTS.

4 1. Measuring inbreeding depression at a sequence of stages (e.g., Dudash 1990, Johnston 1992; Slides 10-11). Inbreeding depression can vary dramatically from one life stage to the next. Fitness of selfed and outbred progeny can be estimated and compared at a sequence of life stages, enabling the investigator to assess the unfolding of inbreeding depression. 2. Trait values as a function of inbreeding coefficient (detection of epistasis). In a longitudinal experiment, inbreeding and trait means are monitored over a series of generations. In the absence of epistasis, the trait mean should show a linear decline with increased inbreeding (Slide 7). Curvilinearity of provides a test for contributions from epistasis. In the ideal experiment, inbreeding is conducted in multiple, independent lines. A deviation from linearity might be caused by a systematic effect (epistasis) but it could also arise as a stochastic effect (sampling artifact and autocorrelation with a line). One can distinguish between these two alternatives using replicate lines. 3. Many small replicate populations (Lynch 1988b - see later lecture on experimental studies of evolution). Theoretical predictions are available for the mean and variance of a phenotypic trait across a series of populations of finite size that differentiate in the absence of selection. Note that in theory based on the additive model for phenotypic value (variance among lines = tg/n e ), lines do not go extinct because of inbreeding, their means merely fluctuate without drifting downard. In other words, the trait mean does not steadily decline. This theory provides the forumla used in R programming assignment 2 REFERENCES GENERAL BACKGROUND *Charlesworth, D. & B. Charlesworth Inbreeding depression and its evolutionary consequences. Ann. Rev. Ecol. Syst. 18: *Crow, J. F. & M. Kimura An Introduction to Population Genetics Theory. Burgess Publ. Co., Minneapolis. Darwin, C The Effects of Cross- and Self-fertilization in the Vegetable Kingdom. Murray, London.{paperback version available from Univ. Chicago Press} Darwin, C The Variation of Animals and Plants under Domestication. Murray, London. {paperback version available from Univ. Chicago Press} *Falconer, D. S. & T. Mackay Introduction to Quantitative Genetics. 4th ed. Longman, Essex. **Lynch, M. & B. Walsh Genetics and Analysis of Quantitative Traits. Sinauer, Sunderland. *Wright, S Evolution and the Genetics of Populations. Vol. 3. Experimental Results and Evolutionary Deductions. Univ. Chicago Press, Chicago. THE EVOLUTION OF DOMINANCE Charlesworth, B The struggle for dominance. Curr. Biol. 8:R502-R504. Fisher, R. A The possible modification of the response of the wild type to recurrent mutation. Amer. Nat. 62: Fisher, R. A Two further notes on the origin of dominance. Amer. Nat. 62:

5 Fisher, R. A The evolution of dominance: a reply to Professor Sewall Wright. Amer. Nat. 63: Wright, S Fisher's theory of dominance. Amer. Nat. 63: Wright, S The evolution of dominance: comment on Dr. Fisher's reply. 63: INBREEDING DEPRESSION AND PLANT MATING SYSTEMS Charlesworth, D. & B. Charlesworth Inbreeding depression with heterozygote advantage and its effect on selection for modifiers changing the outcrossing rate. Evolution 44: Dudash, M. R Relative fitness of selfed and outcrossed progeny in a self-compatible, protandrous species, Sabatia angularis L. (Gentiananceae): a comparison of three environments. Evolution 44: Holsinger, K. E Inbreeding depression doesn't matter: the genetic basis of mating-system evolution. Evolution 42: Johnston, M. O Effects of cross and self-fertilization on progeny fitness in Lobelia cardinalis and L. siphilitica. Evolution 46: Lande, R. & D. W. Schemske The evolution of self-fertilization and inbreeding depression in plants. I. Genetic models. Evolution 39: Levin, D. A Inbreeding depression and proximity-dependent crossing success in Phlox drummondii. Evolution 38: Levin, D. A The effect of inbreeding on seed survivorship in Phlox. Evolution 45: Lloyd, D. G Some reproductive factors affecting the selection of self-fertilization in plants. Amer. Nat. 113: Lloyd, D. G Benefits and costs of biparental and uniparental reproduction in plants. pp IN: B. Levin and R. Michod (eds.). The Evolution of Sex: An Examination of Current Ideas. Sinauer. Lynch, M The genetic interpretation of inbreeding depression and outbreeding depression. Evolution 45: Morgan, M. T Adaptive structures and the stability of hermaphroditic sex expression in flowering plants. Evolution 46: Nagylaki, T A model for the evolution of self-fertilization and vegetative reproduction. J. theor. Biol. 58: Ritland, K. 1990a. Genet identity and the genetic demography of plant populations. Pp IN: A. H. D. Brown et al., Plant Population Genetics, Breeding, and Genetic Resources. Sinauer, Sundeland.

6 Ritland, K. 1990b. Inferences about inbreeding depression based on changes of the inbreeding coefficient. Evolution 44: Schemske, D. W. & R. Lande The evolution of self-fertilization and inbreeding depression in plants. II. Empirical observations. Evolution 39: Schoen, D. J Relative fitnesses of selfed and outcrossed progeny in Gilia achilleifolia (Polemoniaceae). Evolution 37: Schoen, D. J. & M. T. Clegg Estimation of mating system parameters when outcrossing events are correlated. Proc. Natl. Acad. Sci. USA 81: Shaw, D. V. & R. W. Allard Estimation of outcrossing rates in Douglas-fir using isozymes. Theor. Appl. Genet. 62: INBREEDING DEPRESSION IN ANIMALS Bittles, A. H. & E. Makov Inbreeding in human populations: an assessment of the costs. pp. xxxx, IN: C. G. N. Mascie-Taylor and A. J. Boyce (eds.). Human Mating Patterns. Cambridge Univ. Press. Crow, J. F. & M. J. Simmons The mutation load in Drosophila. pp. 1-35, IN: Ashburner, M., H. L. Carson & J. N. Thompson (eds.), The Genetics and Biology of Drosophila. Vol. 3c, Academic Press, London. Greenwood, P. J., P. H. Harvey & C. M. Perrins Inbreeding and dispersal in the great tit. Nature 271: Harvey, P. H. & K. Ralls Do animals avoid incest? Nature 320: O'Brien, S. J., M. E. Roelke and L. Marker Genetic basis for species vulnerability in the cheetah. Science 227: O'Brien, S. J., D. E. Wildt and M. Bush East African cheetahs: evidence for two population bottlenecks? Proc. Natl. Acad. Sci. USA 84: O'Brien, S. J., J. S. Martenson and C. Packer Biochemical genetic variation in geographic isolates of African and Asiatic lions. Natl. Geog. Res. 3: Ralls, K., K. Brugger & J. Ballou Inbreeding and juvenile mortality in small populations of ungulates. Science 206: Schull, W. J. & J. V. Neel The Effects of Inbreeding on Japanese Children. Harper & Row, New York. Simmons, M. J. & J. F. Crow Mutations affecting fitness in Drosophila populations. Ann. Rev. Genetics 11: Slatis, H. M An analysis of inbreeding in the European bison. Genetics 45:

7 Thornhill, N. W The Natural History of Inbreeding and Outbreeding. Univ. Chicago Press, Chicago. INPUT OF POLYGENIC MUTATION TO QUANTITATIVE TRAITS Lynch, M. 1988a. The rate of polygenic mutation. Genet. Res. Camb. 51: RESEMBLANCE AMONG RELATIVES IN POPULATIONS WITH PARTIAL SELFING Wright, A. J Additive variance and average effect with partial selfing. Genet. Res. Camb. 50: EXPERIMENTAL DESIGN AND DATA ANALYSIS Lynch, M. 1988b. Design and analysis of experiments on random genetic drift and inbreeding depression. Genetics 120: Weir, B. S Genetic Data Analysis II. Sinauer, Sunderland, Mass. NUMBER OF MATING PARTNERS AND SEXUAL SELECTION Arnold, S. J. 1994a. Is there a unifying concept of sexual selection that applies to both plants and animals? American Naturalist 144:S1-S12. Arnold, S. J. 1994b. Bateman's principles and the measurement of sexual selection in plants and animals. Amer. Nat. 144:S126-S149. Arnold, S. J. and D. Duvall Animal mating systems: a synthesis based on selection theory. Amer. Nat. 143: Jones, A. G., et al The Bateman Gradient and the cause of sexual selection in a sex-role-reversed pipefish. Proc. Roy. Soc. Lond. Biol. Sci. 267: Jones, A. G., et al Validation of Bateman s principles: a genetic study of mating partners and sexual selection in newts. Proc. Roy. Soc. Lond. Biol. Sci. 269: Jones, A. G., J. R. Arguello, and S. J. Arnold Molecular parentage analysis in experimental newt populations: the response of mating system measures to variation in the operational sex ratio. American Naturalist 164: Meagher, T. R Analysis of paternity within a natural population of Chamaelirium luteum. I. Identification of most-likely male parents Amer. Nat. 128: Williams, C. J. & S. Evarts The estimation of concurrent paternity probabilities in natural populations. Theor. Pop. Biol. 35: