Natural Selection: Secondary article

Jon Seger, University of Utah, Salt Lake City, Utah, USA Article Contents

. Introduction acts strongly on the proportional numbers of male and female offspring . Darwin on the Numbers Game among the progeny of adults. The equilibrium is often one at which males and females are . Conditional Indifference, Not Optimality produced in roughly equal numbers, but under certain ecological and genetic . Cost versus Numbers circumstances there may be dramatic population-wide biases, and even in populations . Benefit Versus Numbers with balanced sex ratios, parents are often selected to produce strongly male- or female- . Mode of Inheritance and Locus of Control biased progenies in response to variations in their individual condition. . Condition-Dependent Strategies . Sex Allocation in

Introduction Darwin on the Numbers Game

Why are approximately equal numbers of male and female In Chapter 8 of The Descent of Man, after a review of sex offspring produced each generation in most species with ratios in mammals, fish, birds and insects, Darwin (1871) separate sexes? A seemingly obvious mechanistic explana- opens a section called ‘On the Power of Natural Selection tion suggests itself in species where sex is determined to regulate the proportional Numbers of the Sexes, and chromosomally, for example by sperm carrying either an X General Fertility.’ Its second paragraph begins as follows or a Y chromosome.In such species, meiotic segregation of (p.316):Let us now take the case of a species producing _ the chromosomes carrying female- and male-determining an excess of one sex – we will say of males – these being genes will give rise to equal numbers of female- and male- superfluous and useless, or nearly useless.Could the sexes determining gametes, and thereby to equal numbers of be equalised through natural selection? We may feel sure, female and male zygotes.But this cannot be a general from all characters being variable, that certain pairs would explanation, because many species with nonchromosomal produce a somewhat less excess of males over females than sex determination also have balanced sex ratios.Con- other pairs.The former, supposing the actual number of versely, biased sex ratios are sometimes produced in species the offspring to remain constant, would necessarily with chromosomal sex determination, demonstrating that produce more females, and would therefore be more the Mendelian mechanism can be overridden.A seemingly productive.On the doctrine of chances a greater number of obvious functional explanation suggests itself in mono- the offspring of the more productive pairs would survive; gamous species where a father and a mother must and these would inherit a tendency to procreate fewer cooperate in brood care to rear more than minimal males and more females.Thus a tendency towards the numbers of offspring (for example, in most passerine equalisation of the sexes would be brought about. _ The birds).But this functional advantage cannot provide a same train of reasoning is applicable _ if we assume that general explanation either, because monogamy is taxono- females instead of males are produced in excess, for such mically restricted and rare while balanced (or approxi- females from not uniting with males would be superfluous mately balanced) sex ratios are widespread and common. and useless. A very general principle of sex-ratio evolution was This passage expresses the most important elements of described by R.A.Fisher in The Genetical Theory of the modern theory as later stated more precisely and Natural Selection (1930).Fisher’s account of the principle generally by Fisher.In the following paragraph (pp.317– is traditionally considered to mark the beginning of 318) Darwin even seems to anticipate the concept of modern understanding of sex allocation, but Edwards parental expenditure or investment (as ‘force’), explicitly (1998) has recently shown that almost all elements of noting the trade-off between offspring number and off- Fisher’s argument can be found in some long-neglected spring quality that now plays a central role in many models works by several late nineteenth and early twentieth of sex allocation.Today we summarize the argument (in its century authors including Darwin.Edwards suggests that simplest form) by noting that members of the minority sex Fisher understood his own account of the principle to be enjoy greater reproductive success than members of the derived from these earlier sources, and that he assumed his majority sex, regardless of the mating system, because interested contemporaries would have been as familiar every offspring must have a mother and a father.Parents with these sources as he was.This may explain why Fisher that produce a relative excess of the underrepresented sex (1930) presents the principle so casually. do not have more offspring than typical parents, but their offspring have more offspring.Parents that overproduce the underrepresented sex will thus enjoy greater than

ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Nature Publishing Group / www.els.net 1 Natural Selection: Sex Ratio average genetic representation in the generation of their authors who have summarized research in this large and grand-offspring. active field.The paragraphs that follow mention just a few major extensions of the basic principle, which has been applied to an amazingly broad (and ever-growing) range of Conditional Indifference, Not situations. Optimality The fitnesses associated with production of male and Cost versus Numbers female offspring are strongly frequency dependent.When equal numbers of males and females are produced in the If offspring of one sex are individually more costly than population at large, the parents of sons and the parents of offspring of the other sex, such that a brood composed daughters enjoy equal representation in the second (and entirely of the more costly sex can include fewer of them, subsequent) generations; parents are indifferent to the then the equilibrium will be one at which the total cost sexes of their offspring, in the sense that no one could do (effort, expenditure, investment) allocated to each sex is better (or worse) by producing any other sex ratio.But if equalized over the population as a whole.To be more the population sex ratio is not balanced, then some precise, if the individual cost ratio is R : 1 (females : males), parental sex ratios (those favouring the underrepresented then the equilibrium numerical sex ratio will be 1 : R, and sex) will produce more grand-offspring than others and the investment ratio will be (R 1) : (1 R) 5 R : R 5 1:1. absolutely more than are produced by any sex ratio in a Thus, more generally, the principle is that net allocation to population with equal numbers of males and females.Thus (investment in) each sex will be equal at equilibrium, even if a balanced sex ratio is an evolutionary equilibrium, not an this means that the numbers of the two sexes will be optimum; it is often considered to be the canonical unequal.For example, males and females are of very evolutionarily stable strategy (ESS). different sizes in some species of wasps and bees (usually This verbal account of sex-ratio evolution makes several females are larger than males), and parents tend to produce simplifying assumptions.For example, it assumes that sons more of the smaller sex (usually males). and daughters are equally costly to produce; that parents This cost-versus-numbers principle can be derived from do not differ in their abilities to produce viable sons and a simple formalization of the basic argument.Because the daughters; and that individuals mate randomly through- summed reproductive success of all females must equal the out the population (or at least that the population is not summed reproductive success of all males, a parent structured differently for males and females).When any of producing f females and m males will have an expected these (or several other) assumptions is relaxed, the fitness (number of grandchildren) proportional to W 5 equilibrium sex ratio can change.In some cases, the (f/F) 1 (m/M), where F and M are the population average equilibrium becomes heterogeneous in the sense that some or total numbers of female and male offspring.If the parents are favoured to produce progeny sex ratios possible progeny compositions for individual parents (f, m) different from those of other parents in the same are constrained by differential costs (R : 1) as defined population; such patterns of differential sex allocation above, then W will be the same for all feasible progeny sex are often expected to reflect variations in individual ratios if and only if the population-wide offspring condition, ecological circumstance, or social status, among productions F and M are in the ratio 1 : R.Otherwise, other factors that may affect the reproductive prospects of individual parents will be able to maximize W by making parents or their offspring. broods consisting entirely of the sex with less net The selection pressures associated with sex ratios are investment over the population as a whole; offspring of very strong, so real species and individuals are expected to this underinvested sex will produce more grandchildren, respond to them.Theorists, field workers, and laboratory per unit investment, than offspring of the overinvested sex. experimentalists have explored hundreds of these possibi- This formal development of the sex-ratio principle has long lities during the last few decades, and this work has yielded been attributed to Shaw and Mohler (1953), but according some spectacularly detailed and convincing analyses of to Edwards’ (1998) account of Fisher’s ‘lost’ sources, a adaptation.Accessible reviews (varying in emphasis and similar equation was derived almost 70 years earlier by scope) are provided by Bourke and Franks (1995), Bull and Du¨ sing (1884).MacArthur (1965) identified a principle Charnov (1988), Bulmer (1994), Charnov (1982, 1993), closely related to the Du¨ sing–Shaw–Mohler formulation, Clutton-Brock (1991), Crozier and Pamilo (1996), Emlen namely that the product of the numbers of females and (1997), Frank (1990, 1998), Godfray (1994), Godfray and males (Nf Nm) is maximized at the equal-investment Werren (1996), Herre et al.(1997), Hewison and Gaillard equilibrium (also see Charnov, 1982; Karlin and Lessard, (1999), Karlin and Lessard (1986), Klinkhamer et al. 1986). (1997), Nonacs (1986), Trivers (1985), Williams (1979), Many factors influence the relative costs of individual and Wrensch and Ebbert (1993), among many other male and female offspring.Indeed, much sex-ratio research

2 ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Nature Publishing Group / www.els.net Natural Selection: Sex Ratio centres on attempts to define and estimate these factors, contain two or fewer sibships, but allocations become 1 which can vary even among closely related species.For nearly balanced (m!2)asn rises beyond more than a few. example, a sex difference in body size may not correspond This model has been extended in many ways and its to a difference in cost if members of the larger sex acquire, predictions have been tested extensively in laboratory through their own effort, the resources needed to support experiments and in the field, mainly in a few groups of their extended growth.Thus gorillas and elephant seals do parasitoid and fig-pollinating wasps like those whose not have notably female-biased numerical offspring sex biologies motivated Hamilton’s analysis.In general, these ratios, as might otherwise be expected.Likewise, differ- tests support the model and show, for example, that female ential mortality of the sexes will not affect the allocation wasps can respond appropriately to cues that indicate ratio if the mortality difference arises after the period of whether a given mating group (at a host or in a fig) will parental investment (Leigh, 1970).This seems counter- contain fewer or more than the typical number of sibships intuitive, since differential mortality may cause strongly (see Herre et al., 1997). biased operational sex ratios among breeding adults.But A related principle applies where females often remain such inequalities are self-compensating, with respect to on their natal territories for life.If sisters compete for a parental sex allocations.Suppose males die at a relatively more or less fixed pool of resources while males disperse high rate after the period of parental investment (as they do widely in search of unrelated mates, then parents may in many species).Then, from a parent’s point of view, the realize diminishing returns on investment in daughters relatively poor survival prospects of a male will be offset, after the first one or few (local resource competition precisely, by his relatively rich reproductive prospects if he (LRC); Clark, 1978), and the equilibrium allocation ratio does survive to adulthood. may be male-biased.Conversely, if sisters (or brothers) Even where factors like self-feeding or differential cooperate in activities that further their reproduction, then mortality are not at issue, there may be large indirect costs parents may realize increasing returns in proportion to that make one sex more expensive than the other.For their investment in the cooperating sex, which may example, a typical honeybee colony produces hundreds of therefore be produced in excess (local resource enhance- times more drones than virgin queens, suggesting that ment (LRE); Emlen et al., 1986). Offspring may also return colonies (and populations) invest more in male than in benefits directly to their parents, for example by remaining female reproductives.But a young queen must inherit a near the parents’ nest and helping the parents rear substantial fraction of her natal colony’s worker force if additional offspring that they would not be able to rear she is to have any chance of founding a successful new on their own.If offspring of one sex are more likely than colony.This large ‘hidden’ cost makes each virgin queen as those of the other sex to remain as helpers at the nest, then expensive as a much larger number of drones, who fly away the effective (net) cost of an offspring of the helping in search of mates from other colonies. (staying) sex is reduced relative to that for the nonhelping (dispersing) sex, and more of the helping sex should be produced, on average.Each of these three resource-based syndromes occurs in at least a few taxonomic groups, Benefit Versus Numbers where they often appear to elicit sex-ratio biases of the expected kinds (Emlen, 1997). Just as the costs of male and female offspring may differ in ways that affect the equilibrium sex ratio, so may several kinds of benefits or payoffs.Hamilton (1967) pioneered research in this area by recognizing that strongly female- Mode of Inheritance and Locus biased sex ratios may evolve where brothers compete with of Control each other for mates.For example, in some groups of insects and mites, offspring mate in small groups composed The models of sex allocation discussed above all assume of one or a few sibships, with the females later dispersing implicitly that offspring sex is controlled by autosomal widely in search of oviposition sites or other resources.In genes in the parent(s).Different outcomes are sometimes this circumstance there may be little advantage, to a parent, expected (and observed) where this assumption does not in producing many more sons than would be needed to hold.For example, genes with unequal probabilities of inseminate all the females in a mating group, because transmission to the two sexes (e.g. those on sex chromo- matings not obtained by one son are likely to be obtained somes or in the cytoplasmic genomes of mitochondria and by another; thus male offspring after the first one produced chloroplasts) are strongly selected to bias offspring become increasingly redundant.The equilibrium propor- production toward the sex that transmits them most tional allocation to males under this simplest model of local efficiently. mate competition (LMC) is m 5 (n 2 1)/2n, where n is the Cytoplasmic male sterility (CMS) frequently appears number of unrelated sibships in a mating group.Strong polymorphically in outbreeding hermaphroditic plants. female biases are expected where typical mating groups Individuals expressing male-sterile mitochondrial geno-

ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Nature Publishing Group / www.els.net 3 Natural Selection: Sex Ratio types produce no viable pollen, but as females they set more expected since workers greatly outnumber the queen and seeds, on average, than do normal hermaphrodites that perform almost all parental investment (Trivers and Hare, invest in pollen.Because cytoplasmic genes are transmitted 1976; Nonacs, 1986; Bourke and Franks, 1995; Crozier and only through seeds, a CMS genotype may increase in Pamilo, 1996).Smaller biases are expected, even if workers frequency when rare, even if it enjoys only slightly greater control their colony’s allocation, where queens mate with than average seed set (Lewis, 1941).However, the nuclear several males; where colonies contain several queens; and genes of male-sterile plants may suffer drastically reduced where workers lay male-destined (haploid) eggs.These fitness by losing all transmission through pollen in predictions are also broadly (but not invariably) satisfied exchange for only modestly increased seed production. by comparative data on allocation ratios.Worker control Thus the evolutionary ‘interests’ of nuclear and cytoplas- of the sex ratio is not absolute, and is expected to depend on mic genes are in conflict, since each genome benefits from a many details of a species’ biology; in principle, queens pattern of sex allocation that reduces the potential might gain partial or complete control at some times in the transmission of the other.Nuclear mutations that restore evolutionary histories of some species. male fertility are therefore expected to increase rapidly in frequency.Such restorers exist, and they are often polymorphic at several different genetic loci within local populations, possibly owing to deleterious side effects Condition-Dependent Strategies suffered by plants that do not carry CMS genotypes and therefore gain no benefits from the restorers (de Haan et al., Developmentally and behaviourally flexible responses to 1997a,b,c; Charlesworth and Laporte, 1998).CMS muta- variable environmental conditions can be adaptive for tions and restorers are expected to exhibit complex many kinds of phenotypic attributes, including sex ratios. dynamics, and geographically separated populations For example, Trivers and Willard (1973) argued that while should diverge rapidly.Genetic analyses often find offspring of both sexes should usually benefit from above- considerable heterogeneity among populations, as ex- average investment (e.g. nutrition in utero or during pected, and higher frequencies of male sterility are some- nursing), one sex might benefit more than the other.If times observed in hybrids between populations or closely so, then parents that find themselves in good condition related species than in crosses within the parental popula- might increase their expected number of grand-offspring tions (Belhassen et al., 1991). by producing more of the sex that benefits more from Just as genomes may ‘disagree’ over sex allocation, so increased investment, while parents in poor condition may individuals, even where their behaviour is controlled would do best to produce more offspring of the other sex, by conventional nuclear genes.There are many such which suffers less from reduced investment.This model has possibilities, but by far the best documented are those been tested many times, especially in ungulates.Under the involving conflict between queens and workers within harem-polygynous mating systems of many ungulate colonies of social Hymenoptera.All members of this insect species, small differences in size, strength and health of order are haplodiploid, with diploid females arising from adult males could have large effects on their mating success, fertilized eggs and haploid males from unfertilized eggs.As so the prediction has usually been that mothers in relatively a consequence, female workers may be more closely related good condition should overproduce males, while mothers to their sisters (including the virgin queens they rear) than in poor condition overproduce females.In only some cases to their brothers.In the simplest, most extreme case, where have the results been as expected, and these mixed findings the colony has a single queen that mated with just one male, have led to debate about the model’s applicability.A recent workers are three times as closely related to the female review finds that maternal investment is most often sex- 3 reproductives reared by their colony (r 5 4) as to the male biased in the most highly polygynous and sexually 1 reproductives (r 5 4).However, the queen is always equally dimorphic species; such a pattern is expected under the 1 related to her sons and daughters (r 5 2).As a consequence, assumptions of the Trivers–Willard model (Hewison and the queen is indifferent to her colony’s sex ratio when the Gaillard, 1999). population’s allocation ratio is 1 : 1, but the workers are Sex-ratio manipulation appears to be common in birds. indifferent when the population-wide allocation ratio is For example, Ellegren et al.(1996) found that broods of 3 : 1 (females : males), because only then will they realize collared flycatchers fathered by males with relatively large equal genetic returns on their investments in reproductive white forehead patches (a character implicated in female sisters (one-third as reproductively successful per unit mate choice) were more male-biased than those fathered by investment, but three times more closely related) and males with small forehead patches.Kilner (1998) found brothers (three times as successful per unit investment, but that zebra finches produced more females when food was only one-third as related) (Trivers and Hare, 1976). available in excess than when food was limited, consistent Allocation ratios have been estimated for many species with previous work suggesting that the reproductive of social Hymenoptera, especially ants, and they indicate success of females depends more strongly than that of that workers tend to prevail in this conflict, as might be males on how well they were fed as nestlings.In many

4 ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Nature Publishing Group / www.els.net Natural Selection: Sex Ratio species of birds, parents that pair and breed early in the of egg-laying queens (Evans, 1995).These findings season have better success, on average, than those that pair demonstrate that workers can estimate the genetic and breed late; seasonal changes in average clutch sex diversity within their colony and then respond by adjusting ratios have been described for several bird species, and the colony’s proportional investment in male and female Daan et al.(1996) suggest that these trends support a reproductives.In at least one species the mechanism Trivers–Willard model in which early clutches emphasize appears to involve variation in the proportion of male- the sex whose subsequent date of first breeding will be destined larvae that are destroyed by workers (Sundstro¨ m accelerated more by an early date of birth. et al., 1996). Why do any queens mate just once, if multiple Dramatic sex-ratio adjustments occur in the Seychelles mating leads to a less-biased colony sex ratio that is more in warbler, Acrocephalus sechellensis (Komdeur et al., 1997). the queen’s interest? One possibility is that multiple mating Females nest once per year and lay just one egg.Daughters entails risks of some kind, that partially offset the fitness often remain on their natal territory, but sons disperse.On gains from a more favourable colony sex ratio; if so, then a high-quality territory, an adult daughter’s help increases these risks would appear to be substantial. the parents’ probability of fledging an offspring, but on a low-quality territory, a daughter may actually lower her parents’ fitness.Parents on low-quality territories over- produce sons, and those on high-quality territories over- Sex Allocation in Hermaphrodites produce daughters, unless they already have two resident helpers, in which case they produce 93% sons.These large The theory of sex allocation extends in straightforward sex-ratio adjustments cannot be explained, even in ways to simultaneous and sequential hermaphrodites principle, by differential mortality of offspring produced (Charnov, 1982, 1996).The male gametes of partially in roughly equal (Mendelian) proportions, because females self-fertilizing simultaneous hermaphrodites experience lay just one egg.In birds, females are the heterogametic sex, local mate competition (LMC) and, as expected, many which suggests that mothers may be able to bias the self-fertilizing species show strikingly reduced develop- segregation of sex chromosomes in meiosis, or that they ment of male reproductive structures.The male gametes of may be able to detect the sex of eggs shortly after meiosis is outbred simultaneously hermaphroditic animals may also completed and then resorb or ‘dump-lay’ those of the experience LMC, to the degree that a given clutch of eggs is undesired sex and quickly form another egg, until the likely to be fertilized by sperm from a single mating partner desired sex is obtained (see Anderson et al., 1997; Emlen, (Fischer, 1984; Charnov, 1996; Petersen and Fischer, 1997). 1996); species meeting this assumption often bias alloca- There has also been much theoretical and empirical tion strongly toward female function (Fischer, 1981; work on conditional sex-allocation strategies in Hyme- Petersen and Fischer, 1996).Sequential hermaphrodites noptera.Responses by parasitoid and fig-wasp females to often change sex in response to changed mating opportu- variable levels of local mate competition were mentioned nities, as expected from general principles of condition- above.In social species with a single queen who may have dependent sex allocation. mated once or several times, the average relatedness of In many hermaphroditic plants, major investments in workers to their reproductive sisters will vary because some male function (pollen and pollinator attraction) occur will be half-sisters in those colonies where the queen mated before major investments in female function (seed and fruit more than once; on the other hand, a worker’s relatedness set).Considerable vegetative growth may occur between to her reproductive brothers is unaffected by the queen’s these phases of sex allocation.To the extent that early male mate number.Boomsma and Grafen (1990, 1991) pointed investments diminish opportunities for later growth (and out that if workers could determine whether their mother hence for resource acquisition made possible by larger had mated once or several times, then they should adjust size), male function may entail a ‘hidden’ cost that is not their sex allocation so that many or most of the once-mated revealed in comparisons of resource flows to male and (high-female-relatedness) colonies produce only female female functions.Such opportunity (growth) costs of male reproductives, while many or most of the twice-mated function may help to explain why many outbreeding plants (low-relatedness) colonies produce only male reproduc- appear to make larger investments in female than in male tives. function, and why gynodioecious sexual systems (where Bimodal distributions of colony sex allocation (‘split sex populations contain some pure females in addition to ratios’) are seen in many species (Nonacs, 1986), and this hermaphrodites) are more common than androdioecious variation has recently been shown to correlate with the systems (where populations contain males and hermaph- queen’s mate number in a few species where mate numbers rodites) (Seger and Eckhart, 1996; Klinkhamer et al., 1997; were estimated from genetic markers (Sundstro¨ m, 1994; Eckhart and Seger, 1999). Sundstro¨ m et al., 1996). Split sex-ratio distributions have In hermaphrodites, as in bisexual species, sex ratios also been found in species where intracolony relatedness affect and are affected by many aspects of biology and asymmetries vary because colonies have different numbers individual circumstance.The ‘Power of Natural Selection

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