November 4, 2009 Bioe 109 Fall 2009 Lecture 17 The evolution of mating systems. The evolution of sex ratio

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1 November 4, 2009 Bioe 109 Fall 2009 Lecture 17 The evolution of mating systems The evolution of sex ratio - let us define sex ratio as the proportion of males to females. - in discussing the evolution of sex ratio, it is important to distinguish between the two distinct sex ratios: 1. the population sex ratio 2. the individual sex ratio (the sex ratio of progeny from a female) - in most sexually-reproducing species, males and females are produced in equal numbers giving a 1:1 sex ratio. - in many species, this is an inevitable consequence of chromosomal mechanism of sex determination. - one sex is homogametic (XX), the other is heterogametic (XY). - the evolution of sex chromosomes is responsible for this system. - sex chromosomes have evolved independently in different animal groups. - in birds and some insect species like butterflies, males are the homogametic (ZZ) and females are heterogametic (WZ). - the existence of sex chromosomes does not guarantee the a 1:1 sex ratio - some species which have sex chromosomes have evolved sex ratios that differ from unity. - this indicates that selection can act to influence sex ratio. - in some instances, one would expect strong selection pressure for this to occur. - for example, consider the northern elephant seal. - males control large harems of females in which they monopolize matings. In elephant seals, all females that survive to breeding age have the potential to breed whereas in males, only about 10% get a chance to control a harem in their lifetime. - from the point of view of the species, a 1:1 sex ratio appears maladaptive. A much better one would be a ratio of 1 male to 9 females. - natural selection does not act for the good of the species, however, but for the benefit of the individual. - it was Fisher in 1930 who provided a genetic explanation for the evolution of a stable sex ratio of 1:1. - Fisher realized that because every individual has a mother and a father, females and males must contribute equally, on average, to subsequent generations. - therefore, males and females must have the same average fitnesses. - what we see in the case of the northern elephant seal is a case in which the variance in fitness in males is much larger than females. - however, the mean fitness of the two sexes is the same.

2 - Fisher realized that in a population that has more males than females, it is advantageous for an individual female to produce a biased sex ratio favoring daughters. - however, the fitness advantage would not be realized in the first generation but in the second when the daughters produce granddaughters! - if a mutation causing a biased female sex ratio enters the population, it will thus increase in frequency. - once it reaches a high frequency, there is now an excess of females, so it is no longer selectively favored. - if a new mutation producing a male-biased sex ratio occurs, it will be favored by selection. - the stable equilibrium point of this system is for a 1:1 sex ratio. - this is a classic form of frequency-dependent selection. - Fisher s theory can only be tested when there is genetic variation in individual sex ratio. - one species in which such variation exists is the platy Xiphophorus maculatus in which there are three types of sex chromosomes W, X, and Y. females: XX males: XY WX YY WY - this leads to some interesting results when different types of males and females are crossed. - there are six possible crosses between males and females. - four crosses lead to 1:1 sex ratios. - the cross between XX and YY individuals leads to 100% sons (XY). - the cross between WX and XY leads to a 3:1 ratio of females to males. XX x YY 100% XY male WX x XY 25% WX female 25% WY female 25% XX female 25% XY male - Basolo (1994) tested the prediction of sex allocation theory by setting up two populations of platys that differed in the initial frequencies of males and females. Pop 1: 0.15 WX females Pop 2: 0.15 WX females 0.60 XX 0.07 WY 0.15 YY males 0.78 XY males 0.10 XY - within two generations the sex ratios in both had fallen to this is consistent with predictions from theory. - there have been two important extensions to Fisher s theory.

3 1. Local mate competition (Hamilton 1967) - Hamilton proposed this modification of sex allocation theory to account for female-biased sex ratios commonly found in small groups of related individuals that have descended from a single foundress. - some of the best examples here come from parasitoid wasps that lay their eggs in other insect species. - in parasitoid wasps, emerging individuals commonly mate with each other. - in this situation, Hamilton realized that it would be advantageous for females to invest in much smaller number of sons, since producing more than needed to inseminate the females would be a waste. - thus, strongly biased sex ratios are commonly found in this type of species - females invest much more heavily in producing daughters than sons. 2. The Trivers & Willard (1973) hypothesis - also called condition-dependent sex allocation. - Trivers and Willard pointed out that in species where females invest heavily in caring for their young, effects of this early investment sometimes are sustained into adulthood. - a mother who is an exceptionally good provider may thus produce larger, or healthier, individuals when they mature into adulthood. - Trivers and Willard proposed that in such species females in extremely good condition should invest more heavily in producing sons than daughters. - this is because the condition typically matters more to a male than to a female. - sexual selection typically affects males much more strongly than females and thus a male in superior condition, because of his mother s assistance, would have a strong fitness advantage. - condition-dependent sex allocation has been observed in a variety of mammals, including humans. Species that change sex - there are two types of hermaphrodites: simultaneous and sequential. - many species of mollusks, crustaceans, platyhelminthes and fish are simultaneous hermaphrodites. - they are capable of producing both male and female gametes either at the same time, or at different periods of their lives. - one selection pressure that may favor the evolution of hermaphroditism is the difficulty in finding a mate. - many simultaneous hermaphrodites are sessile, live at relatively low densities, or are parasitic. - hermaphrodites gain one important advantage in that they do not bear a cost of mating. - there are two forms of sequential hermaphroditism. - in protandrous species - individuals begin life as males and switch to females later in life. - in protogynous species - individuals begin life as females and switch to males later in life.

4 - sex changes of this type occur when there are changes in fitness in one or both sexes as individuals grow in size. - there are three outcomes. 1. No sex change - if reproductive success increases equally with body size in both sexes then there is no selection for sex change. 2. Protogyny - if large size confers success in male competition for females then protogyny is favored. - protogyny and is usually characterized by males being larger and less numerous than females. - an example of a protogynous species is the blue-head wrasse. - Bob Warner (at UCSB) has studied the blue-headed wrasse for many years. - a switch occurs between initial-phase and terminal-phase males once these fish reach a certain size. - initial phase males resemble females and spawn in groups. - terminal phase males are brightly colored and defend territories. - the advantage of being a large terminal phase male is that you can defend a territory and control access to females. - there are two routes to becoming a terminal phase male. - one is from a initial-phase to a terminal phase male. - the second is from a female to a terminal-phase male. - Warner has shown that females switch to become terminal-phase males at about the same size as initial phase males. 3. Protandry - protandry is selectively favored when the reproductive success of males does not increase with size as rapidly as it does for females. - larger females typically produce larger quantities of eggs than smaller females. - in protandrous species males are commonly smaller than females. - protandry is fairly common in invertebrates - for example oysters. - it is also common in plants, a good example here being jack-in-the-pulpits. - jack-in-the-pulpits can produce either male or female flowers at any stage but are much more likely to be female if they are large or exist in a resource-rich environment. - the development of seeds and fruits imposes additional costs on females (resulting in higher energy costs to reproduction than males). - because larger plants can photosynthesize more and store more resources than smaller plants it is advantageous for sexual function to change with size. The evolution of inbreeding and outbreeding - many species of plants can both self-pollinate and outcross. - we can assess the degree to which these two forms of reproduction occur in natural populations by simply measuring departures from Hardy-Weinberg equilibrium.

5 - recall that one of the many assumptions of H-W is that mating be at random. - selfing is a form of non-random mating - it will result in deficiencies of heterozygotes. - the magnitude of heterozygote deficiency can be used to estimate the degree of selfing vs. outcrossing in the entire population. - clearly this indirect method cannot tell us the extent to which individual plants self or outcross. - it can only provide an estimate of the population level of selfing. - many plants try to avoid selfing since this is a form of inbreeding. - many traits have evolved in plants to avoid selfing. - these include: 1. asynchronous male and female functions - e.g., pollen shed after or before plant s stigmas are receptive. 2. monoecy - male and female flowers are separated on the same plant. 3. dieocy - sexes are separated in different individuals. 4. self-incompatibility loci - these loci have evolved to prevent inbreeding - pollen sharing an allele in common with the stigma on which it lands cannot successfully grow a pollen tube. - this results in strong frequency dependent selection - alleles are favored when rare and disfavored when common. - the equilibrium state commonly results in large numbers of alleles present at roughly equal frequencies 5. heterostyly - heterostyly is a polymorphism first studied by Darwin in which either two (distyly) or three (tristyly) forms of flowers exist in a species on different plants. - Darwin did experiments to show that pollen is more effectively transferred between rather than within morphs. - heterostyly thus serves to maximize outcrossing. - in contrast to these traits that favor outcrossing, many plants have evolved characteristics that ensure self-fertilization. - these include reductions in: 1. size of the flower. 2. scent and markings that attract pollinators. 3. pollen production. 4. asymmetry in anther and stigma length.

6 - in its most extreme form, flowers may become cleistogamous and not open at all. - why inbreed? - inbreeding is harmful in the short term but after deleterious genes are purged from a species population, fitness can equal or even exceed the initial outcrossing population. - Fisher pointed out that a partial selfer has a strong selective advantage over an exclusive outcrosser. - this is because it can transmit its genes in three ways: 1. through its ovules 2. through its pollen by selfing 3. through its pollen by outcrossing. - this assumes that the pollen cost to selfing is low, the cost of producing selfed and outcrossed progeny is equal, and that all offspring have equal fitnesses. - another advantage of selfing is reproductive assurance. - if pollinators are scarce, then a plant can produce at least some seeds by selfing.

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