Leonard Nunney

The influence of mating system and overlapping generations on effective population size

The effective population size (Ne) depends strongly on mating system and generation time. These two factors interact such that, under many circumstances, Ne is close to N/2, where N is the number of adults. This is shown to be the case for both simple and highly polygynous mating systems. The random union of gametes (RUG) and monogamy are two simple systems previously used in estimating Ne, and here a third, lottery polygyny, is added. Lottery polygyny, in which all males compete equally for females, results in a lower Ne than either RUG or monogamy! Given nonoverlapping generations the reduction is 33% for autosomal loci and 25% for sex‐linked loci. The highly polygynous mating systems, harem polygyny and dominance polygyny, can give very low values of Ne/N when the generation time (T) is short. However, as T is lengthened, Ne approaches N/2. The influence of a biased sex ratio depends on the mating system and, in general, is not symmetrical. Biases can occur because of sex differences in either survival or recruitment of adults, and the potential for a sex‐ratio bias to change Ne is much reduced given a survival bias. The number of juveniles present also has some influence: as the maturation time is lengthened, Ne increases.

Assessing minimum viable population size: Demography meets population genetics

The discussion of a populations minimum viable size provides a focus for the study of ecological and genetic factors that influence the persistence of a threatened population. There are many causes of extinction and the fate of a specific population cannot generally be predicted. This uncertainty has been dealt with in two ways: through stochastic demographic models to determine how to minimize extinction probabilities; and through population genetic theory to determine how best to maintain genetic variation, in the belief that the ability to evolve helps buffer a population against the unknown. Recent work suggests that these two very different approaches lead to very similar conclusions, at least under panmictic conditions. However, defining the ideal spatial distribution for an endangered species remains an important challenge.

Increased sexual activity reduces male immune function in Drosophila melanogaster

Despite the benefits of resistance, susceptibility to infectious disease is commonplace. Although specific susceptibility may be considered an inevitable consequence of the co-evolutionary arms race between parasite and host, a more general constraint may arise from the cost of an immune response. This “cost” hypothesis predicts a tradeoff between immune defense and other components of fitness. In particular, a tradeoff between immunity and sexually selected male behavior has been proposed. Here we provide experimental support for the direct phenotypic tradeoff between sexual activity and immunity by studying the antibacterial immune response in Drosophila melanogaster. Males exposed to more females showed a reduced ability to clear a bacterial infection, an effect that we experimentally link to changes in sexual activity. Our results suggest immunosuppression is an important cost of reproduction and that immune function and levels of disease susceptibility will be influenced by sexual selection.

Understanding and Estimating Effective Population Size for Practical Application in Marine Species Management

Effective population size (N(e)) determines the strength of genetic drift in a population and has long been recognized as an important parameter for evaluating conservation status and threats to genetic health of populations. Specifically, an estimate of N(e) is crucial to management because it integrates genetic effects with the life history of the species, allowing for predictions of a populations current and future viability. Nevertheless, compared with ecological and demographic parameters, N(e) has had limited influence on species management, beyond its application in very small populations. Recent developments have substantially improved N(e) estimation; however, some obstacles remain for the practical application of N(e) estimates. For example, the need to define the spatial and temporal scale of measurement makes the concept complex and sometimes difficult to interpret. We reviewed approaches to estimation of N(e) over both long-term and contemporary time frames, clarifying their interpretations with respect to local populations and the global metapopulation. We describe multiple experimental factors affecting robustness of contemporary N(e) estimates and suggest that different sampling designs can be combined to compare largely independent measures of N(e) for improved confidence in the result. Large populations with moderate gene flow pose the greatest challenges to robust estimation of contemporary N(e) and require careful consideration of sampling and analysis to minimize estimator bias. We emphasize the practical utility of estimating N(e) by highlighting its relevance to the adaptive potential of a population and describing applications in management of marine populations, where the focus is not always on critically endangered populations. Two cases discussed include the mechanisms generating N(e) estimates many orders of magnitude lower than census N in harvested marine fishes and the predicted reduction in N(e) from hatchery-based population supplementation.

FLUCTUATING POPULATION SIZE AND THE RATIO OF EFFECTIVE TO CENSUS POPULATION SIZE

The effective size of a population (Ne) quantifies the rate at which genetic diversity is eroded by genetic drift (i.e., 112Ne per generation), a fundamental process of evolutionary change. Genetic diversity and its rate of decay have been linked with key components of population fitness (Allendorf and Leary 1987; Ralls et al. 1988; Briscoe et al. 1992; Newman and Pilson 1997; but see Britten 1996). Ne is thus a central parameter both in studies aimed at understanding evolution (Falconer and Mackay 1996) and in the field of conservation genetics (Lande and Barrowclough 1987; Nunney and Campbell 1993; Nunney and Elam 1994). Unfortunately, accounting for all factors that influence Ne is notoriously difficult (reviewed by Caballero 1994). This difficulty is apparently responsible for significant disagreement between theoretical (Nunney 1993) and observed values of the ratio, Ne/N (Frankham 1995). Here we investigate whether this disagreement can be reconciled by incorporating the effect of a factor long known to reduce Ne, namely temporal fluctuations in population size (FPS; Wright 1938). More specifically, we consider the extent to which Ne/N is depressed by FPS over the range of fluctuations observed in wild animal populations. In addition, we present a method for predicting Ne/N from a standard measure of population variability, and we discuss the implications of this theoretical relationship. Several factors affect the effective size of a population: fluctuations in size, variance in fecundity, sex ratio, and the degree to which generations overlap (Crow and Kimura 1970). One difficulty in estimating Ne is that no single formula simultaneously accounts for all these factors. This difficulty would be largely inconsequential if the ratio Ne/N were known to fall consistently within a narrow range. Estimating Ne would be trivial because N is often relatively easily estimated. Theoretical and empirical studies have searched for such a range of Ne/N. Theoretical studies have explored the plausible range of Ne/N through analysis of a reparameterized version of Hills (1972) expression for Ne (Nunney 1991, 1993, 1996). This reparameterization provides several advantages. Ne is expressed in parameters that are biologically interpretable, and for which typical ranges are known. In addition, the parameters can be estimated from data commonly available from single-season studies of real populations (Nunney and Elam 1994). Through thorough numerical exploration of the parameter space, these studies led to the conclusion that Ne/N is usually close to 0.5 and only rarely outside the range 0.250.75 (Nunney 1991, 1993, 1996; hereafter, referred to as the theoretical expectation.) In contrast with this theoretical expectation, a review of 192 empirical estimates (based on a variety of demographic and genetic methods) revealed that Ne/N was usually less than 0.5 (Frankham 1995; hereafter, referred to as empirical estimates.) In fact, approximately one-third of the Ne/N estimates were less than 0.25, and a subset of these estimates (37 from animal taxa) accounting for all factors that influence Ne had an average Ne/N of 0.15 (median = 0.08). By contrast, a subset of estimates (27 from animal taxa) accounting for all factors except FPS had an average Ne/N of 0.38 (median = 0.38). The discrepancy between theoretical expectation and empirical estimates may thus be largely attributable to the fact that the theoretical expectation is based on the assumption of constant N. The theoretical expectation may provide a reasonable estimate of the short-term Ne/N, but the longerterm ratio may often be less than 0.25, owing to the effect of FPS. A long-term estimate of Ne that accounts for FPS is obtained by transforming a series of short-term effective sizes (Wright 1938; see also Crow and Kimura 1970; Lande and Barrowclough 1987):

THE RESPONSE TO SELECTION FOR FAST LARVAL DEVELOPMENT IN DROSOPHILA MELANOGASTER AND ITS EFFECT ON ADULT WEIGHT: AN EXAMPLE OF A FITNESS TRADE-OFF

A selection experiment using Drosophila melanogaster revealed a strong trade‐off between adult weight and larval development time (LDT), supporting the view that antagonistic pleiotropy for these two fitness traits determines mean adult size. Two experimental lines of flies were selected for a shorter LDT (measured from egg laying to pupation). After 15 generations LDT was reduced by an average of 7.9%. The response appeared to be controlled primarily by autosomal loci. A correlated response to the selection was a reduction in adult dry weight: individuals from the selected populations were on average 15.1% lighter than the controls. The lighter females of the selected lines showed a 35% drop in fecundity, but no change in longevity. Thus, there is no direct relationship between LDT and adult longevity. The genetic correlation between weight and LDT, as measured from their joint response to selection, was 0.86. Although there was weak evidence for dominance in LDT, there was none for weight, making it unlikely that selection acting on this antagonistic pleiotropy could lead to a stable polymorphism. In all lines, sex differences in weight violated expectations based on intrasex genetic correlations: Females, being larger than males, ought to require a longer LDT, whereas there was a slight trend in the opposite direction. Because the sexual dimorphism in size was not significantly altered by selection, it appears that the controlling loci are either invariant or have very limited pleiotropic effect on developmental time. It is suggested that they probably control some intrinsic, energy‐intensive developmental process in males.

The maintenance of sex by group selection

The traditional group‐selection model for the maintenance of sex is based upon the assumption that the long‐term evolutionary benefits of sexual reproduction result in asexual lineages having a higher extinction rate than sexual species. This model is reexamined, as is a related model that incorporates the possibility that sexual and asexual lines differ in their speciation rates. In these models, the long‐term advantage of sex is opposed by a strong short‐term disadvantage arising from the twofold reproductive cost of producing males. It is shown that once some sexual lines become established, then group selection can act to maintain sex despite its short‐term disadvantage. The short‐term disadvantage is included in the model by assuming that, if asexual individuals arise by mutation within a previously completely sexual species, then the asexuals quickly displace their sexual conspecifics and the species is transformed to asexuality. The probability of this event is given by the transition rate, us. If the value of us varies between lineages, then one of the effects of group selection is to favor groups (i.e., species) with the lowest values of us. This occurs because lines that do convert to asexuality (because of a high us) are doomed to a high rate of extinction, and in the long term only those that do not convert to asexuality (because of a low us) survive. The net result of group selection is that sex is maintained because of its lower extinction rate (or higher speciation rate) and because asexual mutants only rarely arise.

BATEMAN'S PRINCIPLE AND IMMUNITY: PHENOTYPICALLY PLASTIC REPRODUCTIVE STRATEGIES PREDICT CHANGES IN IMMUNOLOGICAL SEX DIFFERENCES

Abstract The sexes often differ in the reproductive trait limiting their fitness, an observation known as Batemans principle. In many species, females are limited by their ability to produce eggs while males are limited by their ability to compete for and successfully fertilize those eggs. As well as promoting the evolution of sex‐specific reproductive strategies, this difference may promote sex differences in other life‐history traits due to their correlated effects. Sex differences in disease susceptibility and immune function are common. Two hypotheses based on Batemans principle have been proposed to explain this pattern: that selection to prolong the period of egg production favors improved immune function in females, or that the expression of secondary sexual characteristics reduces immune function in males. Both hypotheses predict a relatively fixed pattern of reduced male immune function, at least in sexually mature individuals. An alternative hypothesis is that Batemans principle does not dictate fixed patterns of reproductive investment, but favors phenotypically plastic reproductive strategies with males and females adaptively responding to variation in fitness‐limiting resource availability. Under this hypothesis, neither sex is expected to possess intrinsically superior immune function, and immunological sex differences may vary in different environments. We demonstrate that sex‐specific responses to experimental manipulation of fitness‐limiting resources affects both the magnitude and direction of sex differences in immune function in Drosophila melanogaster. In the absence of sexual interactions and given abundant food, the immune function of adults was maximized in both sexes and there was no sex difference. Manipulation of food availability and sexual activity resulted in female‐biased immune suppression when food was limited, and male‐biased immune suppression when sexual activity was high and food was abundant. The immunological cost to males of increased sexual activity was found to be due in part to reduced time spent feeding. We suggest that for species similarly limited in their reproduction, phenotypic plasticity will be an important determinant of sex differences in immune function and other life‐history traits.

Factors influencing the optimum sex ratio in a structured population

W. D. Hamilton (1967, Science 156, 477-488) calculated the optimum sex-ratio strategy for a population subdivided into local mating groups. He made three important assumptions: that the females founding each group responded precisely to the number of them initiating the group; that ail broods within a group matured synchronously; and that males were incapable of dispersing between groups. We have examined the effects of relaxing each of these assumptions and obtained the following results: (1) When broods mature asynchronously the optimum sex ratio is considerably more female biased than the Hamiltonian prediction. (2) Increasing male dispersal always decreases the optimum female bias to the sex ratio, but it is of particular interest that when moderate levels of dispersal are coupled with asynchrony of brood maturation then the optimum strategy is relatively insensitive to changes in foundress number. (3) When females cannot precisely determine the number of other foundresses initiating the group then the optimum strategy is almost exactly the strategy appropriate to a group of average size. These effects can be most easily understood in terms of local parental control (LPC) of the sex ratio. Through LPC a founding female can alter the mating success of her sons by altering the sex ratio of her brood. Asynchrony in the maturation of broods within a group increases the control that a founding female has over the mating success of her sons, whereas male dispersal reduces it. We have shown that the role of LPC and the role of inbreeding, which favors a female-biased sex ratio in haploidiploid species, are independent and that their effects can be combined into a single general formula r = (1-(r2/z2) E(alpha z/alpha r]/(1 + I). The concept of LPC can also be used to interpret two factors which have been proposed to select for the Hamiltonian sex ratios: local mate competition is LPC acting through sons; and sib mating is LPC acting through daughters.

The Effective Size of Annual Plant Populations: The Interaction of a Seed Bank with Fluctuating Population Size in Maintaining Genetic Variation

Many annual plant populations undergo dramatic fluctuations in size. Such fluctuations can result in the loss of genetic variability. Here I formalize the potential for a seed bank to buffer against such genetic loss. The average time to seed germination (T) defines the generation time of “annuals” with a seed bank, and assuming random seed germination, I show that, under otherwise ideal conditions, a population’s effective size (Ne) equals NT, where N is the number of adult plants. This result supports the general principle that lengthening the prereproductive period increases Ne. When adult numbers vary, Ne at any time depends on N and on the numbers contributing to the seed bank in previous seasons. Averaging these effects over time gives \documentclass{aastex} \usepackage{amsbsy} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{bm} \usepackage{mathrsfs} \usepackage{pifont} \usepackage{stmaryrd} \usepackage{textcomp} \usepackage{portland,xspace} \usepackage{amsmath,amsxtra} \usepackage[OT2,OT1]{fontenc} \newcommand\cyr{ \renewcommand\rmdefault{wncyr} \renewcommand\sfdefault{wncyss} \renewcommand\encodingdefault{OT2} \normalfont \selectfont} \DeclareTextFontCommand{\textcyr}{\cyr} \pagestyle{empty} \DeclareMathSizes{10}{9}{7}{6} \begin{document} \landscape