2What causes sexual dimorphism? Sexual dimorphism means that males and females look differentIn many (but not all) sexually dimorphic species, males are larger than females, or males are more brightly colored, or only males have weapons (horns, antlers, etc.), or only males have exaggerated features such as longer feathers, etc.
5Sexual dimorphism in long-tailed widow birds (Fig. 10.3)
6Sexual dimorphism for height in humans (Fig. 10.2)
7Natural selection is not generally a satisfactory explanation for sexual dimorphism If antlers in male deer are naturally selected because they increase survivorship, then why don’t females have them too?How could bright colors or long feathers of some male birds improve their survivorship?
8Sexual selection explains explains sexual dimorphism Sexual selection is selection for access to mates, or, more generally, reproductive successDarwin distinguished between natural selection (which is selection for adaptations to increase the probability of survivorship and eventual reproduction) and sexual selection which is selection for traits that increase mating successThe distinction is useful because sexual selection might select for phenotypes that are not favored by natural selectionSexual selection can be very strong because, in terms of fitness, failing to mate is equivalent to dying young; and if there is heritable variation in traits that affect mating success then we expect them to evolve
9Asymmetries in sexual reproduction – 1 (Bateman 1948, Trivers 1972) If sexual selection is to explain differences between sexes, it must act differently in the two sexesEggs (or pregnancies) are more expensive than ejaculatesMothers generally invest more resources in each offspring than do fathersIn more than 90% of mammals, females provide substantial parental care and males provide little or noneEven in species with no parental care, eggs are more expensive than sperm, and there are fewer of them
10Asymmetries in sexual reproduction – 2 (Bateman 1948, Trivers 1972) A female’s potential reproductive success is relatively small, and her realized reproductive success is likely to be more limited by the number of eggs she can make (or pregnancies she can carry) than by the number of males she can convince to mate with herA male’s potential reproductive success is relatively large (sperm are cheap and abundant), and his realized reproductive success is more likely to be limited by the number of females that he can induce to mate with him than by his ability to produce sperm
11Asymmetries in sexual reproduction – 3 (Bateman 1948, Trivers 1972) Access to mates will be a limiting resource for males but not for females (in most cases)Therefore, sexual selection will be a more potent force in the evolution of males than in the evolution of females (in most cases)In cases where males make greater parental investment than females, we expect sexual selection to be stronger in females
12Testing the assumption of asymmetries in sexual reproduction: newts (Jones et al. 2002) Experimental designMating takes place in ponds where males gather. Females enter ponds, mate and leave. At any time, more males than females in a pond. No parental care from either sex.Captured all newts from a single pond at egg-laying timeInduced females to lay remainder of eggs in labGenotyped all adult males and females and about two dozen offspring from each femaleAllowed them to determine the reproductive success of both males and females (paternity, multiple mating)
13Testing the assumption of asymmetries in sexual reproduction: newts (Jones et al. 2002) Results Most males did not mate, and therefore had no offspringNumber of offspring per male strongly correlated with number of matesAll females matedNumber of offspring per female not significantly correlated with number of males that she mated withThese observations confirm our assumptions about sexual asymmetry. Male reproductive success is strongly limited by access to females, but female reproductive success limited more by the number of eggs she can make
14Asymmetries in sexual reproduction in rough-skinned newts (Jones et al Asymmetries in sexual reproduction in rough-skinned newts (Jones et al. 2002) (Fig b,c)
15Testing the assumption of asymmetries in sexual reproduction: pipefish (Jones et al. 2000) Experimental designMales provide all parental care (brood eggs). Females can make a clutch of eggs faster than males can brood themGroups of males and females allowed to mate in laboratoryMating success determined by genotyping
16Testing the assumption of asymmetries in sexual reproduction: pipefish (Jones et al. 2000) Results Females more likely than males to not mateFemales more likely to benefit from multiple matesThese result support the assumption that the sex with greater reproductive investment is a limiting resource. When males are a limiting resource for females, variance in reproductive success is higher for females, and we expect sexual selection to be stronger on females than on males.
17Asymmetries in sexual reproduction in broad-nosed pipefish (Jones et al. 2000) (Fig. 10.5 e, f)
18Behavioral consequences of asymmetric limits on fitness Males should be competitiveFor males, reproductive success is limited by access to females. Therefore males are likely to compete for access to females = intrasexual selectionFemales should be choosyIf female fitness is not limited by opportunities to mate, females can afford to be, and should be, choosy. Female choice may enhance fitness if chosen males have “good genes” = intersexual selectionNote: these predictions assume that the female makes a greater reproductive investment than the male
19Sexual selection by male – male competition CombatSperm competitionInfanticide
20Male combatTypically selects for morphological traits, such as large size and weaponryExample: marine iguanasMales are larger than femalesMales provide no parental careFemales mate only once per reproductive season and lay 1 clutch of 1-6 eggs/yr (~20% of body mass). No parental care beyond guarding eggs for a few daysMales fight for territories on basking rocks – threats, chasing, head pushing, fights, bites
21Mating success in male marine iguanas (Trillmich, 1983) (Fig. 10.10)
22Mating success in male marine iguanas Combat for territories favors larger males, and not all territories are created equalMales that obtain copulations are larger than males that don’tMale #59, who obtained 45 copulations, was the largest maleThis is directional selection for large malesWhat limits the size of males?
23Natural selection on body size in marine iguanas – 1 (Wikelski and Trillmich 1997) (Fig. 10.8) Asterisks mark maximum size at which iguanas were able to maintain body weight in two different years
24Natural selection on body size in marine iguanas – 2 (Wikelski and Trillmich 1997) (Fig. 10.8) Size of iguanas is affected by stabilizing natural selectionAppears to be due to availability of food – large individuals can’t get enough food to maintain their body weightMaximum body size at which iguanas could sustain their weight was close to the optimum for survivalMaximum size in females was close to the optimum for survivalBut many males were larger than the optimum for survivalSexual selection drives male size beyond the optimum for survival and male size is limited by a balance between natural and sexual selection
25Sperm competitionSperm competition can occur when the ejaculates of two or more males interact in the female reproductive tractMediterranean fruit flies (Ceratitis capitata) – number of sperm transferred during copulation is greater if other males are present: 3,520 ± 417 vs. 1,379 ± 241Adaptations for sperm competition include:Mate guardingProlonged copulationCopulatory plugsPheromones to reduce female attractivenessSperm removal (damsel flies)Spermicide
27Male – male competition by infanticide LionsMale lions that take over a pride often kill nursing cubs already presentCauses females to return to reproductive state soonerEnhances reproductive success of new males at the expense of previous males
28Sexual selection by female choice Selects for male ornamentation, courtship displays, nuptial giftsExample: barn swallows (Møller 1988, 1991)Males set up territories in breeding coloniesMales attempt to attract mates by displaying tails while perching and flyingFemales lay one or two clutches of eggs during the breeding seasonFemales incubate eggs, both parents feed chicksSwallows are sexually dimorphic particularly for outermost tail feathers, which are longer in males
29Female choice in barn swallows – 1 (Fig. 10.16 b) (Møller 1991) Hypothesis: the longer tail feathers of male barn swallows are the result of female preference for longer tailed males
30Female choice in barn swallows – 2 (Møller 1988) Experimental design: 44 males caught after establishing territories but before mating, and divided into 4 groupsShortened tail feathers by clipping out central portion and re-gluing tipsClipped but not shortened (Control I)Unaltered (Control II)Lengthened tail feathers by adding middle portions taken from (1)
31Female choice in barn swallows – 3 (Møller 1988)
32Female choice in gray tree frogs (Hyla versicolor) (Fig. 10.20) Females prefer males who give longer calls (Gerhardt et al. 1996, Bush et al. 2002)
33Is female choice adaptive? Consideration of asymmetries in sexual reproduction indicates that females are not limited by access to mates, and that females can afford to be choosy, and should be choosy if choice increases their fitnessFemale choice is commonWhat do choosy females get? Is choice by females adaptive?Good genes hypothesis for female choiceSexually selected male traits are indicators of male genetic quality and choosy females are obtaining good genes for their offspring
34A test of the good genes hypothesis in gray tree frogs – 1 (Welch et al. 1998)
35A test of the good genes hypothesis in gray tree frogs – 2 (Welch et al. 1998)
36A test of the good genes hypothesis in gray tree frogs – 3 (Welch et al. 1998) Table 10.3 Fitness of the offspring of long-calling male frogs vs. short-calling male frogsNSD = no significant difference; LC better = offspring of long-calling males performed better than offspring of short-calling males19951996Fitness measureHigh foodLow foodLarval growthNSDLC betterTime to metamorphosisMass at metamorphosisLarval survivalPostmetamorphic growth—
37Calling by male tree frogs is energetically expensive (excerpt of an interview with H. Carl GerhardtGerhardt - Treefrog Choice“So when a male gray tree frog calls for three or four hours the aerobic metabolic rate is going up something like twenty times resting. It’s really the equivalent of running a marathon. And they’re doing this night after night for a long season. And so, it’s an indicator for the physical, energetic cost that this male is investing in his courtship. So this could be something useful for the female, especially if only the fittest males were able to sustain this energetic cost for a very long time. Well, it turns out in gray tree frogs, at least we can show that in fact the female gets something from this choice. Because they do prefer males that give longer than average calls. …. (W)e found, in fact, that the offspring of the long calling males grew faster and grew larger and metamorphosed, that is became little frogs sooner than the offspring of the short calling males. Clearly, the males with the longer calls that were showing, in fact, that they were physically fit also had some genetic fitness which the female was able to benefit from”
38Choosy females may benefit directly through acquisition of resources – 1 Hanging flies (Bittacus apicalis) (Thornhill 1976)Males provide captured insects as “nuptial gifts” to femalesIf female accepts gift, she will copulate with the male while eating the giftLarger gift means longer copulation and more sperm transferThe gift provides the female with food and reduces her own need to hunt for food (and may reduce her mortality)
39Choosy females may benefit directly through acquisition of resources – 2 (Fig b,c) (Thornhill 1976)
40Runaway selection: an alternative model for female choice – 1 R. A. Fisher (1915) – elaborate male traits and female preference for them are the result of a non-adaptive runaway selection process (“fashion-driven selection”, “sexy son” hypothesis)Initial conditions (using tail-length in birds as a typical trait):Male tails are “short” but variable and heritableMost females express a preference for longer tails for some reason (pre-existing sensory bias, good genes, genetic drift) and female preference is heritableBecause of female preference, males with longer tails will leave more offspring
41Runaway selection: an alternative model for female choice – 2 Because male tail-length is heritable, average male tail-length increasesThe offspring of long-tailed males will carry alleles for long tails (in males) and alleles for preference (by females) for long tails (i.e., alleles for longer tails and for preference for longer tails become associated by assortative mating)Therefore the greater reproductive success of longer-tailed males increases both the frequency of alleles for long tails and the frequency of alleles for female preference for long tails, which further increases the reproductive success of long-tailed males, which further increases the frequency of alleles for female preference for longer tails, etc.That is, there is a positive feedback between female preference for a male trait and the exaggeration of that trait.
42Runaway selection: an alternative model for female choice – 3 Sexual selection increases tail length until opposing natural selection prevents further increasesIn contrast to “good genes” models, female choice does not function to enhance the “quality” of her offspringHowever, once female choice becomes widespread, it tends to remain in a population. An unchoosy female who mates with a shorter-tailed male will have sons that have shorter tails, and who will have lowered reproductive success (because most females will choose longer-tailed males)Therefore, the benefit that choosy females do get is that their sons are more sexy than the sons of unchoosy females.
43Can we distinguish between a good genes explanation and a runaway selection explanation for female choice in any particular case? – 1Good genes predicts that offspring of choosy females will have higher survivorship (or some other enhanced non-reproductive fitness component) than the offspring of non-choosy femalesGood genes predicts that male “quality” should be heritable (otherwise choosy females would leave average quality offspring and would receive no benefit from being choosy)Good genes predicts that the male indicator trait that females are choosing (e.g., call length in gray tree frogs) should be costly (otherwise low quality males could cheat and there would be no advantage to choosy females)Runaway selection predicts that the male trait that females are choosing should be heritable (otherwise choosy females will not have sexy sons and will gain no advantage from being choosy)
44Can we distinguish between a good genes explanation and a runaway selection explanation for female choice in any particular case? – 2Good genes predicts that there should be a genetic correlation between offspring genetic quality (fitness) and the male indicator trait that females are using for choice (as appears to be the case in gray tree frogs where longer-calling fathers have fitter tadpoles)Runaway selection predicts that there should be a genetic correlation (association) between the male trait that females are choosing and female preference for that trait
45Stalk-eyed flies: an example of runaway sexual selection Stalk-eyed flies: an example of runaway sexual selection? (Wilkinson & Reillo 1994) – 1In both sexes, eyes are carried at the ends of stalks, and male stalks are longer than female stalksNeither sex cares for youngExperimental test of the prediction under runaway selection that there should be a genetic correlation between chosen male phenotype and female preference for that phenotype – fathers with longer eyestalks will tend to have daughters that prefer longer eyestalks, and fathers with shorter eyestalks will tend to have daughters that prefer shorter eyestalks
47Stalk-eyed flies: an example of runaway sexual selection Stalk-eyed flies: an example of runaway sexual selection? (Wilkinson & Reillo 1994) – 2Experiment:Artificially select on males for longer or shorter eyestalks (13 generations)Then assess preferences of females from the selected linesIf there is a genetic correlation, then females from lines that were selected for longer eyestalks in males should prefer males with longer eyestalks, and females from lines that were selected for shorter eyestalks in males should prefer shorter eye stalksGive groups of 5 females a choice between a long-stalked and a short-stalked maleResults:The predicted correlation was observed (but female choice does not seem very strong for either experimental group)
48Stalk-eyed flies: an example of runaway sexual selection Stalk-eyed flies: an example of runaway sexual selection? (Wilkinson & Reillo 1994) – 3
49Stalk-eyed flies: an example of runaway sexual selection Stalk-eyed flies: an example of runaway sexual selection? (Wilkinson & Reillo 1994) – 4The situation in stalk-eyed flies is more complicated than we have described herein nature, females are about twice as abundant as males, which means that the fitness of the average male is twice that of the average femalelong-stalked males tend to have more sons than daughterstherefore, females that mate with long-stalked males will tend to have more sons, which will increase the fitness of choosy females because they will have more grandchildren than unchoosy females or females who choose short-stalked femalesSee Wilkinson, G.S., D.C. Presgraves, and L. Crymes Male eye span in stalk-eyed flies indicates genetic quality by meiotic drive suppression. Nature 391(Jan. 15):276.
50Sexual selection by female choice – final comments Female choice for good genes and sexy sons (runaway selection) are not mutually exclusiveIf a male trait is heritable and if it indicates good genetic quality, then both types of selection can operate simultaneously
51Is sexual selection “reversed” when sex-roles are reversed? If sexual selection theory is correct, we expect that female – female competition and male choice might be found in species in which males invest more in reproduction than do females, and in which female reproductive success is more limited by access to males than vice versa.In broad-nosed pipefish, in which males brood young and in which females can yolk up eggs faster than males can brood them, these conditions hold, and sexual selection is stronger on females than malesIs there male choice in pipefish and do females compete for access to males?
52Asymmetries in sexual reproduction in broad-nosed pipefish (Jones et al. 2000) (Fig. 10.5 e, f)
53Male choice experiments in pipefish (Fig. 10.28a)
54Male choice in the pipefish Nerophis ophidion (Fig. 10.28 b, c) Females are larger than malesFemales have dark blue stripes and skin folds on their belliesIn male choice experiments, males showed a preference for larger females and females with larger skin foldsFemales showed no tendency to discriminate between males of different sizes
55Male choice in the pipefish Syngnathus typhle (Fig. 10.28 d, e) Females and males similar in size and appearanceFemales can change color to intensify zigzag pattern on their sidesFemales compete over access to males and display dark colors while doing soIn male choice experiments, males prefer to mate with females that have fewer black spots (which are indicative of parasites)Choice is adaptive for males because females with fewer parasites lay more eggs
56Sexual selection in plants - 1 The seed parent (female) must produce a fruit – therefore, the seed parent may make a greater reproductive investment per seed than does the pollen parent (male)Access to seed parents is more likely to limit reproductive success of pollen parents than vice versaIn animal pollinated plants, access by pollen parents to seed parents is via pollinatorsTherefore, the reproductive success of pollen parents is limited by pollinatorsSexual selection on pollen parents should favor adaptations that increase the number of pollinator visits to male flowers – leads to sexually dimorphic flowers with male flowers more attractive to pollinators
57Sexual selection in plants - 2 The showiest part of a flower is the perianth (= sepals + petals)The perianth serves not only to attract pollinators but also to protect reproductive structures when the flower is developing in the budPredictions:If protection is the only function, then the sex with the larger reproductive structure should have the larger perianthIf pollinator attraction is important, we expect at least some species in which male reproductive structures are smaller than female structures to nonetheless have larger male perianthsResults:In wind-pollinated plants (a) was true in 11 of 11 casesIn animal pollinated plants (b) was true in 12 of 42 cases overall (and 12 of 22 cases in which the male reproductive structures were smaller than female reproductive structures)
58Patterns of sexual dimorphism in plants with separate male and female flowers (Fig a) (Delph et al. 1996)This group is consistent with sexual selection as the cause of flower dimorphism
59Sexual selection in plants - 3 Prediction:When sexual dimorphism occurs in floral structures of animal pollinated plants, we expect male “investment” to be greater than female “investment”Results:The prediction is true when male investment is measured by number of flowers per inflorescence and strength of floral odor, but not by quantity of nectar.
60Patterns of sexual dimorphism in plants with separate male and female flowers (Fig b) (Delph et al. 1996)
61Sexual selection in humans is difficult to study Sexual dimorphism in body size in humans: Is it due to sexual selection?Sexual selection in humans is difficult to studyCan’t do the kinds of experiments that we can with animals and so we must often rely on observed correlationsCultural norms and practices, including religious beliefs, may be much more decisive in determining mating behavior
62The “opportunity” for sexual selection is stronger in men than in women (Fig. 10.32) Variation in reproductive success of Kipsigis men of Kenya is greater than that of women; male reproductive success more likely to be limited by access to mates than is female reproductive success; therefore sexual selection should be stronger in males than in females (Borgerhoff Mulder 1988)
63Taller men have more children – an observation that is consistent with sexual selection by female choiceIn study of 3,201 Polish men, married men were likely to be taller than unmarried men, and men who had at least 1 child were taller than men who had no children.Differences are small but statistically significant (except for men in their 50’s) (Pawlowski et al. 2000)
64More evidence that female choice favors tall men In a study of the West Point class of 1950 (Mueller & Mazur 2001), the tallest men had more wives, and younger second wives, and as a result had more childrenWomen who are slightly shorter than average tend to have the most children = stabilizing natural selection on women (Nettle 2002)
65On the other hand….Perhaps we just inherited our sexual dimorphism from our sexually dimorphic ancestors (McHenry 1992)