Biology 441. Animal Behavior

Lecture 21. Monday, 18 November 1996

ANNOUNCEMENTS

1. For Wednesday, read "Batmom's daily nightmare" by McCracken and Gustin (1987. Nat. Hist. 87 (10):66-72) on reserve.

2. Sign up for oral presentations.

3. Midterm II's will be returned Wednesday.

SEX

Why Not

Biparental sexual reproduction is a process by which two individuals make equal genetic contributions to offspring; the offspring thus share only half of the mother's and half of the father's genes. Parthenogenesis (development of an unfertilized ovum) is one of several ways to reproduce asexually -- the mother provides all the genetic material to the offspring. The whiptail lizard genus (Cnemidophorus) of the southwestern U.S. includes several sexual species and several parthenogenic strains, e.g., C. uniparens. (Females of the parthenogenic strains actually still mate, alternating male and female roles.)

Consider a parthenogenetic mutant in a sexual species. She will replicate her genes at twice the rate of sexual females if she has the same reproductive success. George Williams called this disadvantage of sexual reproduction the cost of meiosis.Since sexual females provide only half as many of their genes to offspring, they would appear to be at a selective disadvantage in competition with conspecific parthenogens. Why isn't parthenogenesis more common?

Sexual reproduction also entails the break up of successful genotypes and recombination of their elements. Consider a female human who is heterozygous for sickle cell anemia and thus resistant to malaria If she could reproduce parthenogenetically, producing diploid ova, all of her offspring would have normal hemoglobin and would be resistant to malaria. Yet, if she reproduces with a male heterozygote, 1/4 of their offspring will have sickle cell anemia and 1/4 will be susceptible to malaria.

A third cost of sexuality is the cost of mating (time and energy used for finding a mate, courtship, etc.). In asexual species, time and resources can be invested directly in offspring.

Why?

Most biologists believe that the evolutionary benefit of sexual reproduction must reside in recombination and crossing over. Insofar as the variability which is necessary for evolutionary change depends not so much on new mutations but more commonly on novel combinations of preexisting alleles, sexual populations can respond more readily to changing selection pressures.

Furthermore, most mutations are probably neutral, but some definitely are deleterious. When a mutation occurs in an asexual lineage, all descendents are stuck with it. Muller evoked the image of a rachet wheel (Muller's rachet), clicking irreversibly as deleterious allele after deleterious allele becomes incorporated within any parthenogenetic strain through time. Asexual reproduction provides no means of eliminating mutational errors except through extinction of lineages. In various invertebrates which alternate between sexual and asexual reproduction, experimental imposition of repeated asexual reproduction results in an accelerating decline in fitness and eventual extinction in laboratory populations, apparently due to accumulation of deleterious mutant alleles.

Muller's rachet provides an explanation for the long-term advantage of sex. However, is sex an ESS (evolutionarily stable strategy) in terms of immediate fitness? How do sexual populations resist invasion by parthenogens? In species which exhibit both sexual and asexual reproduction, sexual reproduction seems to be timed when future conditions are uncertain, e.g., once a colonized habitat is saturated and dispersal is the key to future success. Many parasitic species reproduce asexually during a population explosion within a host individual but then reproduce sexually to produce dispersing offspring (.e.g, liver flukes).

Leigh van Valen based his explanation for sex on a line from Alice in Wonderland. One of Alice's strange experiences through the looking glass was her encounter with the Red Queen who took her by the hand and led her on a wild run. When they stopped they were right where they had started; the Red Queen explained, "now here you see, it takes all the running you can do to keep in the same place." Van Valen has argued that within biotic communities any species' gain is somebody else's loss. For example, if gazelles run faster, or hyenas become more effective at hunting gazelles or a new strain of lion distemper arises, lions will be at a disadvantage. Thus, members of each species are in a coevolutionary arms race with their predators, prey, parasites or hosts, and competitors. Like Alice, they have to keep running (evolving) to stay in place. Genetic diversity in offspring may be valuable in thwarting coevolutionary antagonists, particularly pathogens such as bacteria and viruses, which are short-lived and can evolve relatively rapidly compared to their hosts. A parthenogenetic mother would be dooming perpetuation of her genes if she inadvertently passed along her own genotype and a complement of pathogens uniquely adapted to it. There are many invertebrate species in which males disappear at higher latitudes where there are fewer pathogens.

SEX RATIO

For most vertebrates sex determination is determined chromosomally, and half the gametes of the heterogametic sex (e.g., females in birds, males in mammals) would be expected to contain the chromosome for female (or male) traits due to the process of meiosis. Recent studies of green turtles and alligators show that sex is determined by temperature in those species. Higher temperatures produce more females in green turtles. In alligators, eggs incubated at higher temperatures in marshy areas are larger hatchlings and become females, who inherit marsh home ranges; male hatchlings are small and occur in more open-water habitats (Ferguson and Joanon. 1982. Nature 296:850-853). Such ability to vary the sex ratio according to ecological conditions may be important in adapting to spatiotemporal variation in the likelihood that male and female offspring will survive and reproduce. As we shall see, such variability can occur even in mammals which have rigid chromosomal sex determination.

Why do parents produce roughly equal numbers of male and female offspring? In many species several females could be bred by a single male, so why not produce mainly females and cut down on superfluous males? Imagine a population in which females greatly outnumber males. If a particular female is about to produce an offspring and most other females are producing daughters, which sex should it be? Since every future offspring in the population will have a mother and a father, she should produce a male because a son will, on average leave more offspring than will a daughter in such a population because he will likely mate with several females once he has matured. Thus, the sex ratio will generally tend towards unity.

Sir Ronald Fisher argued that parents should produce equal numbers of sons and daughters if the cost (in terms of future reproduction) is the same. The reason is that the mean reproductive success of each sex is inversely proportional to its frequency in the population. If the sex ratio of young at independence deviates from 50:50, those individuals producing more of the rarer sex will have higher expected reproductive success. This is an excellent example of frequency dependent selection.

What if the cost of producing offspring of one sex is more than that of producing offspring of the other sex? In this situation Fisher theorized that the sex ratio which equalizes overall investment in sons and daughters will be stable. Thus, if it takes two years to raise a son but only one year to raise a daughter (so that two could be raised in those two years), a 33:67 sex ratio would be evolutionarily stable. At this ratio the average expected reproductive success of sons is twice that of daughters (since daughters are twice as common), thus balancing the higher cost of producing sons.

Verme (1983. J. Wildl. Manage. 47:573-582) examined the relationship between the sex ratio at birth and fecundity (numbers of fawns/adult doe) of the genus Odocoileus. Among sampled populations, there was an inverse relationship between the percentage of male fawns (ranging from 0.36 to 0.75) and fecundity. Verme suggested that undernourished does tend to produce an excess of males (which disperse) and thus fewer daughters (which stay on the same range and compete with their mothers). Apparently, the physiology of the female's reproductive tract is altered by nutrition so that transport of Y-bearing sperm is favored when females are in poor nutrition states. This makes adaptive sense because males disperse and may find better quality ranges, but females would be competing for food on the same poor quality range. This skewing of the sex ratio is called "local resource competition" (e.g., see Caley and Nudds. 1987. Am. Nat. 129:452-457).

In species in which one sex costs less to raise than the other sex, a numerical excess of the less costly would be expected when parental care is terminated. Clutton-Brock, Albon, and Guiness (1982. Nature 300:178-180) evaluated the sex ratio hypothesis for red deer. In red deer and in many mammals with matrilocal societies, the sex ratio of offspring at weaning favors males (red deer: 118 males:100 females), suggesting that daughters are more costly to produce . A son disperses from the core area of his mother's home range between the ages of 2 and 4 years. Hinds in large matrilocal groups have lower fitness than those in smaller groups: hinds in large groups begin reproducing later in life and have lower fecundity. Thus daughters compete with their mothers for resources, reducing the reproductive success of their mothers Because production of daughters reduces long-term reproductive prospects of mothers, selection could favor mothers who produce male-biased sex ratios. On the other hand, hinds invest more heavily in sons than in daughters before weaning. Hinds raising sons are less likely to calve the following year, and, if they do calve, they calve later than do hinds of similar condition (age) producing daughters. Thus, sons are more costly to produce than daughters up to the time of weaning, but thereafter daughters impose a greater cost. Thus, perhaps the sex ratio initially is biased in favor of males because on average they require less investment, i.e., reduce the future fitness of mothers less than do daughters.

Sex ratio and dominance status

Social status also seems to affect the sex ratio of offspring in mammals. Within groups, dominant females are able to gain access to the best feeding sites while they are pregnant and lactating and have a disproportionately larger share of sons, while subordinate females tend to have daughters.

Gomendio et al. (1990. Nature 343:261-263) summarized findings for relationships between dominance rank and sex ratio of offspring in red deer and primates. In both instances the sex ratio of offspring is associated with dominance status. In red deer dominant females produce more sons than daughters. Dominant females that produce sons outcompete other females for high quality forage so that their sons are competitively superior. Thus, only dominants can effectively raise competitive sons. In primates this pattern is reversed: dominant females conceive more daughters than sons. Daughters of subordinates are harassed by higher ranking females and are at a big competitive disadvantage because dominance rank of females is transmitted from mother to daughter. Since dominant females produce more daughters, itís advantageous to subordinants to produce sons to balance the sex ratio. These examples suggest that there is frequency dependent selection on the sex ratio within social groups in both red deer and primates.

Differential mortality after independence should have no effect on the sex ratio at independence, because within the sex with higher mortality, the survivors will have proportionately higher success, and the average expected reproductive success will still be equal between the sexes. If one sex costs less to raise than the other, then relatively more offspring of that sex should be produced. For example, if males cost twice as much as females to raise to independence, twice as many daughters should be produced. In humans sons have a higher probability of mortality before independence than do daughters. A human mother who loses an offspring will start raising her next offspring sooner. Consequently, sons cost less than daughters (recall that cost means the adverse effect of producing a particular offspring on the parent's ability to produce other offspring). In humans the sex ratio at birth is skewed in favor of sons, in accord with Fisher's prediction.

Differential investment

If variance in reproductive success is greater in one sex than in the other, e.g., in greater males than females (see below), then quality of offspring of the former sex will be particularly important for reproductive success in terms of grandsons and granddaughters. Trivers and Willard theorized that allocations of parental care should be skewed to the sex affected most.

Inbreeding and local mate competition

Equal investment in sons and daughters is based on the assumption that mating is random within the population. In some macrophagous mites young reach sexual maturity while still in their mother's body, with the males completing their life cycle and fertilizing their sisters before being released by the mother. Thus sons mate with daughters while theyíre still within their mother! Macrophagous mite broods typically consist of dozens of females and only a few males. A female will maximize her fitness by releasing the greatest number of fertilized daughters -- she should produce only enough sons to guarantee that all the daughters are fertilized. Since extra sons would only compete with other sons for a limited number of mating opportunities, there is local mate competition. A mother's fitness does not increase linearly as the number of sons increases because sons compete among themselves for local mates (sisters).

Stenseth (1978. Oikos 30:80-89) has studied the wood lemming (Myopus schisticolor). He has hypothesized that inbreeding (both sister-brother and daughter-father matings) is very common during major portions of the breeding cycles of microtine rodents and that during phases of inbreeding the sex ratio is extremely biased in favor of females. Inbreeding apparently coincides primarily with the trough and early increase phases of population cycles, and those lineages producing just enough sons to fertilize daughters will contribute most to the increase, i.e., will have the highest fitness. Further testing of the applicability of this hypothesis on different microtines will be necessary before any general statement can be made.

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