Testing Sensory Bias. Why are females choosy? Sensory Bias. Sensory bias. 1. Direct benefits. 2. Runaway sexual selection. 3.
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1 Why are females choosy? 1. Direct benefits 2. Runaway sexual selection 3. Sensory bias 4. Good genes Sensory Bias 1. Runaway sexual selection predicts females can have preferences for male traits that have no fitness effects (except in generating sexy sons). 2. Burley (1988) glued a feather on top of the heads of some male zebra finches and long-tailed finches. 3. Females preferred the males with artificial crests, even though they don t exist in the species! 4. Thus, females may have innate preferences for certain male traits. Sensory bias 1. Sensory bias hypothesis: Males manipulate the females sensory system, which results in certain male traits spreading in the population. 2. Tungara frogs: Tungara male frogs have a whine and a chuck part of their call. 3. Females love the chuck, but this attracts bats which eat the frogs = tradeoff between natural and sexual selection). 3. Males still chuck because the female s hearing is highly stimulated with deep chucks. This is the case even in a closely related species with no chucks. Testing Sensory Bias How to test for sensory bias 1. Test for preference in females in closely related species that doesn t have the trait. 2. This tells you if the ancestor may have had the preference. 3. Male swordtails have elongated caudal fin which females prefer. 4. The most closely related species without swords are platyfish. 5. Female platyfish also prefer males with swords, when an artificial sword is glued to a male s tail. 6. Key feature: Preference evolves before trait, as detected using a phylogeny.
2 Good Genes 1. The runaway process is especially likely when the male trait is favored by natural selection. RA Fisher 2. Good Genes Hypothesis: Females may prefer certain males because they have good genes that will be passed to their offspring. a. Females get indirect benefits = higher offspring survival. b. Good genes are for some aspect of survival and reproduction rather than for purely attracting females as in runaway selection 3. Females are able to choose good genes by assessing indicator traits in males. 4. Want honest indicators = reliable signals of good genes. a. Handicap Hypothesis: only males in good health are able to produce costly traits. b. Revealing Signal Hypothesis: Only males resistant to parasites will be able to display conspicuous traits. Handicap hypothesis 1. Zahavi (1975) suggested that elaborate male traits are a handicap to day-to-day survival and that females prefer them exactly because they re a handicap. 2. The handicap trait therefore acts as an honest indicator of a male s genetic quality (i.e. males cannot cheat on the signal because it is costly to make). 3. Females select for good genes by selecting males with elaborate handicap traits. Revealing Signal Hypothesis 1. Hamilton and Zuk (1982) proposed that female preferences are often for choosing mates that are resistant to disease. a. Disease is widespread so could apply to many animals. b. Disease also continually evolves new varieties so it presents new selective hurdles. 2. Male traits can indicate good genes for fighting parasites/disease. a. General good health and freedom from parasites are often strikingly indicated in plumage and fur, particularly when these are bright rather than dull or cryptic. --Hamilton and Zuk (1982) b. Vigor is also conveyed by success in fights and by the frequently exhausting athletic performances of many displaying animals. 3. Thus, only males resistant to parasites will be able to display conspicuous traits. Testing for Good Genes 1. Test: Offspring of individuals with good genes indicator traits have increased survival or reproductive success. These are indirect, genetic benefits to female fertility. 2. Female gray tree frogs prefer males that give long calls. 3. Welch et al., 1998 took the eggs laid by a particular female and fertilized half with sperm from a long calling male, and half with sperm from a short calling male. a. Thus, could control for genes of the female by comparing sibs. 4. Long calling males produced larvae that can survive and grow better than short calling males.
3 Testing the good genes hypothesis 1. Petrie et al. (1991) tested whether the number of eyespots in a male peacock s tail signaled his genetic quality. 2. First showed that number of eyespots predicted a male s mating success. Also, cutting off eyespots led to lower reproductive success in males. 3. Experiment: Females paired with random males, eggs collected and chicks raised in common environment. 4. Offspring of males with more ornamented tails grew better and had higher survival to age two when released into wild. Testing Hamilton-Zuk Hypothesis 1. Hamilton-Zuk hypothesis predicts that only males that are disease-free will be able to fully develop elaborate trait. 2. Male three-spined sticklebacks develop bright red coloration and build nests where females come to spawn. Males care for the eggs for ~10 days so females want to be sure the male is healthy enough to care for and protect the eggs. 3. Females prefer to mate with males with more intense red coloration a. Prefer redder male under normal white light (panel b left) but have no preference under green lights (red color not visible, panel b right). b. Male courtship display not affected by lighting experiment, so preference due to coloration. Testing Hamilton-Zuk Hypothesis 4. Male s red coloration signaled his physical condition (redder males have greater mass per unit length). 5. When preferred bright males infected with parasites, both condition and coloration decline. a. Under white light females no longer preferred them but under green light males parasitization no effect on female choice. 6. Females benefit from choosing males redder males because they are in better condition to take care of eggs and better able to resist parasite infections. Summary 1. There are many reasons why females may prefer particular males. Need to test alternative hypotheses to determine which one applies. 2. Multiple hypotheses may apply for a particular trait. a. Red color in sticklebacks = good parental care (direct benefit) + good genes (indirect benefit). 3. There are often tradeoffs of producing elaborate male traits. a. Increased predation (e.g. tungara frogs). b. Energetically expensive (handicap hypothesis).
4 More complexities in Sexual Selection 1. Sexual selection in females and male choice. 2. Sperm competition 3. Sexual conflict Sexual selection in females 1. Males may be choosy about whom they mate with, especially when they make a large investment in parental care. 2. Sometimes both sexes have similar ornaments. a. Darwin suggested that these could arise via mutual mate choice. b. Could be a correlated response when males evolve ornaments. 3. Example: Male and female crested auklets display most vigorously to members of the opposite sex with longer crests. crested auklets great crested grebes Sexual selection in females 4. Female specific ornaments can be used to advertise female quality to males. a. Female baboons develop large sexual swellings; size is correlated with female quality. b. Females compete for matings with either dominant males (who can protect them/offspring) or with several males (gives many males paternity, which can prevent infanticide). Sexual Role Reversal 1. Obligate sex role reversal a. Male pipefish carry eggs instead of female. Females compete for males and males prefer larger, more ornamental females who produce larger clutches 2. Facultative a. Male katydids produce protein-rich spermatophores for females. b. When food is scarce females compete for males, but when food is abundant males can produce them more quickly and males compete for females.
5 Sex differences in competition 1. Both sexes compete with members of their own sex 2. Females typically compete for access to resources necessary for successful reproduction such as breeding sites, parental care, social rank, etc 3. Males usually compete for access to females; either directly or indirectly through controlling resource females need 4. Eclectus parrots have sexual dimorphism a. Females compete for nest hollows and display below the canopy. Bright red and blue contrast against dark trunks of trees. b. Males compete for females and coloration is trade-off between female attraction and camouflage. Sperm Competition and Cryptic Female Choice 1. Females often copulate with more than one male even though they don t have same relationship between number of mates and reproductive success as males do. 2. This means that sexual selection can occur between sperm. a. Sperm from rival males can compete (~male-male competition). b. Females may choose sperm (~ female choice). 18 Why do females mate with many males? 1. Cost of Resistance a. Female gains no benefit by mating multiply except to avoid harm b. Female dung flies can drown as males struggle for possession 2. Material (or direct) benefits a. Mating with multiple males allows access to more resources b. Example: Females can gain access to resources on territory of male (dragonflies and damselflies). c. Example: May increase the amount of care provided by multiple males to offspring (dunnocks, Galapagos hawks) 2. Indirect benefits a. Fertility insurance: Reduce risk of having infertile partner. Test=look at fertilization success. b. Example: Polyandrous female Gunnison s prairie dogs are pregnant 100% of the time while monogamous females are pregnant 92%. 3. Avoiding male harassment/infanticide a. Males that have a sufficient chance of paternity won t commit infanticide. Why do females mate with many males? 1. Songbirds provide some of the best evidence for females mating multiply to gain genetic benefits. a. Social monogamy doesn t not mean genetic monogamy because female extra pair paternity is common % of young may be sired by male not the female s social mate depending on the species. 2. Females paired to attractive males tend to be more faithful. Females paired to unattractive males (as measured by the trait in table 7.3) actively seek extra-pair matings. Attractive males tend to survive better suggesting that they have good genes. 3. Test: Compare the success of extra-pair sired young with their within-pair sired half-siblings raised in the same nest. a. There is Increased survival of extra-pair sired young in both blue tits and collared flycatchers. Thus, females gain a genetic benefit from extra-pair matings Species Attractive male trait Trait of extra-pair male compared to social mate Reference Great reed warbler Acrocephalus arundinaceus Song repertoire Larger Hasselquist et al. (1996) Barn swallow Hirundo rustica Tail length Larger Saino et al. (1997) Blue tit Cyanistes (Parus) caeruleus Ultraviolet reflectance of crown feathers Brighter Hunt et al. (1999) Kempenaers et al. (1997) Collared flycatcher Ficedula albicollis White patch on forehead Larger Michl et al. (2002) Sheldon et al. (1997) Table 7.3 In some song birds, females seek extra-pair matings from males whose display traits are more elaborate than those of their social mates
6 Consequences of Extra-Pair Mating 1. Extra-pair mating seems to be an important part of sexual selection. Can it explain the evolution of sexually dimorphic traits? 2. Owens and Hartley (1998) compared plumage dimorphism in species with information on rates of extra-pair paternity a. No correlation between degree of plumage dimorphism and number of social mates, but strong correlation between plumage dimorphism and rate of extra-pair paternity. b. Mating opportunities afforded by extra pair matings may help drive diversification in plumage coloration. Extra-Pair Mating 1. Why don t females always pair with their most attractive male? a. When competition for the best mates is intense, females may be forced to settle for an unattractive mate. b. Good genes is just one part of the equation. Having a mate to provide parental care is important. But females may try to optimize both. 2. Constraints on extra-pair matings a. Social mate may reduce level of parental care in response to partner s extra pair mating. i. In experiment where a female collared flycatcher was removed for an hour during her fertile period, her social mate reduced his effort in chick feeding. b. Attractive males sire higher quality sons but poorer quality daughters compared to less attractive males. i. Based on idea of sexually antagonistic genes, where an allele has high fitness in one sex, but low fitness in another. ii. Thus different sires may be best for sons vs. daughters. iii. Sexually antagonistic genes have been found in D. melanogaster and in red deer (Cervus elaphus). Sexual conflict 1. Sexual conflict can occur whenever the optimal outcome of reproductive event is different for males and females. 2. Can lead to each sex evolving adaptations to favor the outcome towards its own interests a. Sexually antagonistic coevolution of traits in males and females 23 Sexual conflict-over mating 1. For a given encounter it will usually pay a male to mate but a female to resist (due to the relationship between # of mates and reproductive success). 2. Male water striders will jump on a female s back, grasp her, and attempt for force copulation. Females are more susceptible to predation and have reduced foraging abilities with a male on her back so already mated females try to avoid males. a. Correlated evolution in male morphology to increase grasping (elongation of grasping genitalia) and female morphology to resist (elongation of abdominal spines). b. Example of adaptations in one sex matched by counter adaptations in the other. 3. The conflict can also go the other way. a. Female songbirds try to gain extra-pair matings; social partner will follow her to try to prevent her from mating with other males.
7 Sexual conflict after mating: male adaptations 1. Male intra-sexual selection continues post-copulation in the form of sperm competition 2. Sperm removal: Female insects store sperm in spermatheca; males will either remove sperm from a previous male or pack it into the corners to ensure their sperm is used to fertilize the eggs 3. Copulatory plugs: Male parasitic worms (Moniliformes dubius) will seal up the reproductive tract of females to prevent them from remating. 4. Altering mating ability of other males a. Male parasitic worms sometimes also seal up the reproductive tract of other males to prevent them from mating. b. Hemipteran insect, Xylocoris maculipennis, mates by males injecting sperm into the body cavity of females. A male can inject his sperm into a rival male. The sperm swim inside the body to the victim s testes where they will be passed onto a female the next time the victim mates. Sexual conflict after mating: male adaptations 5. Anti-aphrodisiacs: Male Heliconius butterflies deposit a substance on the female after mating that discourages other males from mating with her. 6. Sterile sperm: Parasperm are sterile, but are used to delay the remating time of a female by filling up her reproductive tract. 7. Accessory gland proteins (Acps): Male ejaculate contains proteins that influence female behavior and physiology. a. Drosophila melanogaster has at least 80 Acps. b. They increase female s egg laying rate, decreasing her likelihood of remating, incapacitate rival sperm, etc. b. Increase male s reproductive success, but decrease female s lifespan. Sexual conflict after mating: male adaptations 8. Strategic sperm allocation: Even though sperm is cheap to produce males don t have a limitless ability to copulate. a. Adders loose as much body mass during spermatogenesis as when searching and competing for females. 9. Pizzari et al 2002 tested for strategic sperm allocation in feral fowl (Gallus gallus, ie chickens). Females were fitted with a harness that collected sperm that could be counted. a. Males increased sperm investment when there were more male competitors. b. Male allocated more sperm to females with larger combs, which lay larger eggs. c. A male s sperm allocation decreased with repeated exposure to the same female, but renewed with the arrival of a novel female. This has been termed the Coolidge effect. Sexual conflict after mating: female adaptations 1. Females can preferentially choose sperm from specific males to use to fertilize their eggs. This is known as cryptic female choice. 2. When female feral fowls are forced to mate with subordinate males they will eject his sperm immediately after copulation. 3. Experiments by Tregenze et al. on field crickets. a. When female field crickets are mated to two siblings they have a greatly reduced number of eggs that hatch. b. When mated to one sibling and one non-sibling have equal hatching success as females mated to two non-siblings. c. Able to sort the sperm and use only from non-sibling male.
8 Sexual conflict: who wins? 1. Sexually antagonistic adaptations are likely to lead to Red Queen dynamics where neither sex gains a long-term advantage. 2. Antagonistic coevolution demonstrated in Drosophila melanogaster a. Two selection lines created: 3 males and 1 female per vial (intense sexual selection) or 1 male and 1 female per vial (no intra-sexual selection). b. In monogamous line males decreased their courtship and mating rate and female survival and fecundity was greater than in the intense sexual selection line. c. Males evolved to be less harmful to females when guaranteed paternity. d. Females from monogamous line had significantly lower survival and reproductive success when mated to males from intense sexual selection line. e. Thus, monogamous females evolved to be less resistant to harmful male traits compared to females in intense sexual selection line. Sexual conflict: who wins? 1. Post-mating conflicts can also result in coevolution of genital morphology 2. Different species of male waterfowl have phalluses that vary in length from 1.5 cm to 40 cm. Length is correlated with the frequency of extra-pair matings. 3. Females have evolved extra spiral or pouches within their vaginas in response to elongated and elaborate phalluses. 4. Spirals are in the opposite direction to male phallus spirals suggesting antagonistic rather than mutualistic coevolution 30 Chase-away sexual selection 1. Discovery of antagonistic coevolution between sexes led to new model of sexual selection: chase-away sexual selection. Proposed by Holland and Rice (1998). 2. Chase-away sexual selection: males are selected to induce females to male and females then evolve resistance to male tactics/traits. 3. Drosophila selection experiments and waterfowl are examples of chase-away, but the hypothesis can also explain the exaggeration of traits males use to attract females. 4. Swordtails are an example of sensory bias, and also an example of chase-away selection. a. Female platyfish (males don t have swordtail) have stronger preference for males with swordtail than female swordtail fish do. b. Female attraction for swords has declined as swords have evolved as predicted by chase-away. Chase-away sexual selection 1. Chase-away sexual selection can also lead to polymorphisms 2. Ischnura elegans damselflies have one male type, but three color morphs for females: red, yellow and blue. Blue is actually a male-mimic 3. Male mating harassment has favored female counter-adaptions 4. Males form a search image for common females. Frequency-dependent selection causes rare females to have an advantage because they face less harassment 32
9 Summary of Sexual Selection by Female Choice Who Benefits from Sexual Selection? Good Genes Runaway Chaseaway Females + 0/+ - Males - 0/+ + Good Genes: 1. Females get indirect benefits = good genes for offspring survival. 2. Males maintain costly sexual signals and many males may not mate. Runaway: 1. Considered non-adaptive with respect to naturally selected traits. 2. Females may get sexy sons. 3. Males with the trait have high reproductive fitness, but there may be naturally selected costs. Chaseaway: 1. Female reproductive fitness lowered. 2. Male reproductive fitness increased. 3. Continual arms race. Summary 1. Asymmetries in investment leads to different selection pressures in males and females. 2. Sex that invests less is more competitive while sex that invests more is choosier. 3. Strong competition for mates (sexual selection) typically results in intense male-male competition (intra-sexual selection) and females being selective about which males they mate with (inter-sexual selection). 4. Females may prefer males due to either direct benefits, runaway sexual selection, sensory biases, or good genes benefits. 5. When males contribute to parental investment males may be choosy and females may compete for mates. 6. Sexual selection can continue after mating, in the form of sperm competition or cryptic female choice. 7. Sexual conflict and chaseaway sexual selection can occur when one sex tries to increase its fitness at the expense of its partner.
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