Ethology & Behavioural Ecology The Evolution of Reproductive Behaviour Chapter 10 Alcock (Animal Behavior) Tom Wenseleers

Plan of talk Evolutionary origins of two sexes Typical sex roles Reversed sex roles Male-male competition Female choice

Aims & Objectives Aims Objectives Present a simple model for the evolution of male (small gamete) and female (large gamete) roles. How sex differences in parental investment select for typical sex roles (e.g. choosy females) + exceptions Objectives Learn examples Understand the evolutionary logic in the evolution of gamete size differences and typical sex roles

1. Evolutionary origin of two sexes: small gametes (males) & large gametes (females) NOT IN TEXTBOOK!!

Origin of gamete size differences Will the mutant producing smaller gametes be selected for? Model Maynard Smith Assume small gametes are half size and that the mutant can make twice as many as a result. Yes If survival of smaller embryo is >50% that of normal embryo No If survival of smaller embryo is <50% that of normal embryo Note that small embryo is 75% the size of the large embryo, and that when rare (i.e. new mutant) small gametes only fuse with large gametes. We are only considering "invasion" conditions, meaning a rare small gamete mutant in a population making large gametes.

Graphical model The curve represents the survival of the immature individual as a function of the size of the embryo resulting from the fusion of two gametes in an ancestral situation when gametes were of one size.

Graphical model The tangent from the origin shows the size of the embryo,a, that maximises survival per unit mass (ie it maximises y/x for biologically permitted pairs of values of x and y, that is the values on the survival curve).

Graphical model The tangent from the origin shows the size of the embryo,a, that maximises survival per unit mass (ie it maximises y/x for biologically permitted pairs of values of x and y, that is the values on the survival curve).

Graphical model The optimal size of a gamete is half of the optimal size of an embryo.

Graphical model Would making half sized gametes be favoured? Yes. A half size gamete fusing with a normal gamete results in an embryo 75% the normal size with survival b. And making twice as many half size gametes gives more surviving offspring since 2.b > a.

Conclusion The model in the previous slides presents the idea that from an initial situation of equal-sized gametes, it is possible for smaller gametes to be at an advantage. In other words for two sexes to evolve in a sexually reproducing population in which there is initially only one sex. However, the advantage of the smaller gametes will decrease as they get more common if fusion is at random. E.g., if two small gametes would fuse the embryo might be too small to survive. We might expect small gametes to evolve the ability to avoid fusing with each other. This would cause the evolution of two distinct mating types, males and females.

2. The evolution of typical sex roles

Typical sex roles Angus Bateman & Robert Trivers: typical male and female sex roles come about because of sex differences in investment in individual offspring. MALES invest little in each offspring can potentially have large numbers of offspring can greatly increase fitness by having multiple partners rarely can increase fitness by being choosy FEMALES invest a lot (more than males) in each offspring cannot, potentially, have large numbers of offspring cannot greatly increase fitness by having multiple partners usually can increase fitness by being choosy

Angus John Bateman Robert Trivers

Typical sex roles

Males: typically brightly coloured as a result of female choice males are usually more brightly coloured to attract females male female gang gang cockatoo

Males: typically larger as a result of male-male competition males are usually larger and stronger than females male female orangutan

Eager males and choosy females # fertilisable females < sexually active males (♂-biased operational sex-ratio) selects for “eager” males and “choosy” females males should frequently want to mate with females when they don’t want to females should be choosy and reject low-quality males

Coercive sex Iron cross blister beetle Not enforced Long courtship No courtship Struggle Iron cross blister beetle

Traumatic insemination spermalege Male bedbugs have a saber-like penis that they insert directly into the abdomen of their mates prior to injecting them with sperm. Such traumatic insemination may have evolved to overcome female choosiness. Female counterdefence: spermalege (modified region of abdomen where male pierces female).

A counteradaptation to male sexual exploitation simulated penis with sterile needle simulated penis with dirty needle

Another female counterdefence Dunnocks (heggemus): females eject sperm of low-status males An interesting sort of sperm ejection occurs among Dunnocks, small brown birds common in English gardens. Alpha males try to prevent matings by lower-ranking males but are rarely successful. Most Dunnock matings are preceded by a ritual-like phenomenon called "cloaca-pecking." The female raises her tail exposing the cloaca. Instead of mating, the anticipating male pecks at the cloaca, an action that stimulates a pumping action and ejection of a droplet of sperm from previous matings. After the male inspects the droplet, normal mating follows. This bizarre scenario required the coordinated evolution of two different kinds of behavior (male and female) as well as the development of the female's sperm-ejection mechanism. Davies Nature 1983

Females: typically more choosy Clark & Hatfield J. Psych. Hum. Sex. 1989 Males Females “Would you go to bed with me tonight?” “Would you go out with me tonight?”

Females: typically more choosy Clark & Hatfield J. Psych. Hum. Sex. 1989 Males Females “Would you go to bed with me tonight?” 75% 0% “Would you go out with me tonight?” 50% 56% But sex roles still much more equal in humans than in any other primate, because of the large contribution of males in the upbringing of children.

Test: sex role reversal How can we test Trivers' idea that typical sex roles come about because of sex differences in investment in individual offspring? For example, that females are more choosy than males because they invest more in the offspring, and so are limited in the number of offspring by how much they can invest. We predict that there will be sex role reversal in those species where males invest a lot in offspring. For example, because the male provides a costly nuptial gift to the female, or provides costly parental care to young.

Pipefish: males that get pregnant Hippocampus: brood in pouch Syngnathus: brood in pouch Phyllopteryx: brood on tail

Sex role reversal in pipefish Males get "pregnant" and provide oxygen and nutrients to a clutch of eggs held in an egg pouch During the time of male pregnancy females of some species (e.g. Syngnathus scovelli) can produce enough eggs to fill 2 male pouches. Given an even sex ratio, male pouch space is therefore in short supply. Males in these species tend to be sex role reversed, and tend to be choosy (they select females which provide the most eggs) However in other genera, e.g. Hippocampus, the female egg laying rate is limiting. In these there is no sex role reversal.

Sex role reversal in pipefish

Nutritious spermatophores In many insects, the male transfers nutrients with his sperm or provides a resource for the female to eat when mating ("nuptial gift"). This has been much studied in Orthoptera (crickets, grasshoppers).

Sex role reversal in Katydids A female of the Australian Katydid Kawanaphila eats a spermatophore whilst sitting on a pollen-poor kangaroo paw flower.

Sex role reversal in Katydids If the difficulty of making nuptial gifts changes, then this may change choosiness. Males should be more choosy when the resources needed to make the nuptial gift are scarce. This was tested in the Australian Katydid Kawanaphila. Food supply varies greatly through the breeding season. When food is limited to pollen-poor kangaroo paw flowers spermatophores are hard to produce, and so very valuable. The males are often choosy and the females compete for males. But when food is abundant males rarely are choosy and females do not compete for males.

Sex role reversal in Katydids Male Katydids provide a large nuptial gift at mating. Males are choosy when the resources (pollen) needed to make the gift are scarce.

Sex role reversal in mormon crickets Mormon crickets are large, flightless Orthoptera. Males transfer an enormous edible spermatophore to females when they mate as a nuptial gift. Constitutes 25% of a male's body mass.

Sex role reversal in mormon crickets Males transfer an enormous edible spermatophore to females when they mate as a nuptial gift. This constitutes 25% of male's body mass. Males probably can mate only once. Females can produce several egg clutches, provided that they can persuade several males to mate with them. Males put more resources in, so the operational sex ratio is female biased. That is, there are more females looking for males than vice versa. High densities of mormon crickets can form. When this happens, males stridulate. Females come quickly to the male, and jostle to compete for chances to mate with him. Males exercise choice over which females to mate with, preferring larger females who will be more fecund. That is a male chooses a female who will be able to lay more eggs fertilised by his sperm.

Sex role reversal in mormon crickets

Sex role reversal in mormon crickets Being choosy is beneficial for males of the mormon cricket (USA). They mate with larger, more fecund, females.

Sex role reversal: the wattled jacana Male uniparental care Causes male to carry most of the cost of offspring production Results in choosy males and ornamental, eager females Most birds have biparental care, and these do not show sex role reversal There are but two tribes in the world where polyandry is stable, preferred, and regarded as the normative as the normative form of marriage. These are the Todas of southern India and the Marquesans of Polynesia. Among the Todas the preferred form of polyandry is fraternal, that is, the wife marries a series of brothers (cp. the Banyankole of Africa). Only occasionally is the nonfraternal type to be found. Among the Marquesans the nonfraternal form is common. In Toda polyandry several brothers establish a common household with one woman. Paternity of the children is determined by ritual in which one brother presents the wife with a toy bow and arrow and the offdpring following this rite are credited to the husband who executed the ritual. Only when another husband carries out out the bow-and-arrow ceremony does paternity go to him, but again all the children are ascribed to the last husband to carry out the rite, even though he may have been dead for years. Among the Todas polyandry is definitely associated with low economic status. In fact the nobility not infrequently practices polygyny. When the co-husbands are brothers they occupy one house, but in the occasional examples of nonfraternal polyandry they have separate dwellings and the wife rotates her visits among them. In the Marquesas polyandrous marriage is as stable as any other. There is usually a main husband who acts as an agent for his wife in the management of family affairs. The other husbands are not his brothers but the younger sons of families of lower rank, or "male concubines". They are, however, accorded considerable latitude and may leave one household and join another. Here, too, economic conditions are severe. Cultivation is difficult and the islands are subject to periodic droughts leading to crop failures, water shortages, and severe epidemics. Fishing is dangerous and difficult in the deep waters off the mountaineous islands. Given that 80% of all the peoples in the world allow polygynous marriage (Marvin K. Opler, Polyandry, Am.J.Sociol., Sept. 1943) it is extraordinary that an exception such as polyandry exists at all. Everywhere else in Polynesia polygyny is the norm. In the Americas amomng the Indians, polyandry occurred sporadically, frequently taking the form of a temporary union prior to marriage in the Shoshoni tribe. The occurrence of fraternal polyandry amongst the south American Taruro and Cawahib implies an institutionalized practice, but polyandrous families were infrequent. The Caingang, describes as casual in their regulation of sex, had no more than 14% polyandrous marriages. They also provide the only instance of polygandrous, or "group" marriage (barring the north American Oneida community which will be discussed presently), totaling 8% of 308 marriages ( The Encyclopaedia of Sexual Behavior, Vol.1, ed. Albert Ellis & Albert Abarand, London, 1961, p.105). Polyandry is a form of marriage "socially sanctioned and culturally patterned" involving "residential cohabitation as well as sexual rights" (George Peter Murduck, Social Structure, MacMillan, New York, 1949). However, it occurs so infrequently that it may be regarded as an ethnological curiosity. Although some cultural anthropologists have described the occurrence of polyandry in certain north American Indian tribes, this is, strictly speaking, not the case. What has been mistaken for polyandry, Opler notes (Marvin K. Opler, Polyandry), was usually an example of extra-marital sex of a woman with a number of men, sometimes the brothers of her husband. Polyandry is highly infrequent, perhaps because it goes counter to the biological tendency (fallen human nature) of the male to demand exclusive possession of his mate, or because it runs counter to the divine pattern of the patriarchy which the biblically-based Hebrew-Christian theologies subscribe to. As far as the former proposition is concerned, if it is true, then culture counteracts biology when polyandry occurs. The explanation is complex, but an important consideration seems to be the scarcity of women in societies where polyandry is practiced, a scarcity resulting from female infanticide. Among the Todas, for example, the sex-ratio was 127-259 males to 100 females. But why the infanticide? The answer is probably the extreme poverty of the people, resulting from the inhospitable environment. That this is not the sole reason for polyandry is shown by the fact that other societies have as extreme poverty with infanticide, and still others practice infanticide when the poverty is not so great (e.g. abortion amongst Asian women in Great Britain). In the remote Himalayas, where arable land is scarce, fraternal polyandry is practiced, a group of brothers sharing a wife. All the children are regarded as the offspring of the eldest brother. When the brothers die, the estate goes to the sons, who in turn marry one wife. Polyandry seems to be associated with a system of land tenure that prevents fragmentation of already small holdings. There is also a nonfraternal varietry, such as that found among the Marquesans. However, polyandry is very rare and is incompatible with the surplus of women generally to be found in human societies. Emlen et al. 1998

Conflict over sex roles in hermaphrodites: flatworms both want to become the male (minimum investment) "penis fencing": first one who is stabbed by the other’s penis becomes the female and has to produce expensive eggs Pseudobiceros hancockanus Michiels, N.K., and L.J. Newman. 1998. Sex and violence in hermaphrodites. Nature 391(Feb. 12):647

Conflict over sex roles in hermaphrodites: banana slug penis chewing: the one whose penis is bitten off first becomes the female can take 12 hours A.B. Harper 1988, B.L. Miller 2005 Alice Bryant Harper, apophallation Banana slug

Sexual selection Charles Darwin: made a distinction between natural selection (acts on individual survival) and sexual selection (acts on likelihood to mate) intrasexual selection: competition within one sex for mating opportunities, e.g. male-male fights intersexual selection: likelihood to mate affected by interactions between the two sexes, e.g. as a result of female choice

Male ornaments Antlers selected due to female choice male-male competition intersexual competition intrasexual competition European stag beetle red deer quetzal peacock red deer

3. Male-male competition

Male-male competition Male-male competition manifests itself in a wide variety of adaptations on the part of males, many of which have a strong behavioural component. Fighting and selection for large body size Alternative mating tactics alternatives that are equally rewarding alternatives not equally rewarding (best of a bad job) Mate guarding Sperm competition etc... etc...

Fighting

Developmental costs Males of the dung beetle fight for mates. Beetles with long horns (left) have a fighting advantage but tissue that goes into horn construction (blue) is unavailable for the building of eyes (yellow). As a result, males with long horns (left) have smaller eyes than rivals with short horns (right). Both types may well be equally fit.

Body size and mating systems in seals In seals, there is strong correlation between sexual dimorphism and polygyny. The sexes are of similar size in species where males cannot monopolise a large number of females. Where males can monopolise a harem of females, there is an advantage to large male size and this results in greater size dimorphism.

Body size and mating systems in seals Elephant seal males can weigh 2000 kg. They fight vigorously and dangerously. The winner (beachmaster) commands a harem of dozens of females. The other males skulk away and get few or no matings. But maybe in a future year one of them will be the beachmaster. We can show that fighting is to acquire mates by correlating male dominance with mating success.

Body size and mating systems in seals McCann's work on southern elephant seals on South Georgia. Recent DNA analysis shows that mating success is tightly linked with paternity.

Sexual dimorphism Big elephant seals can win fights with other males and thereby get high reproductive success by monopolizing a lot of females. There is therefore tremendous selection pressure on elephant seal males to get large. But it takes a lot of time and energy to get big. We can predict that costly investment in the growth and maintenance of large bodies will only occur when exceptional rewards are accrued by large individuals. Also, there will come a point where there is no longer any individual advantage of growing larger or being more fierce (recall the hawk-dove game). Where mating occurs is also very important. If males cannot access and monopolise many females then extreme dimorphism should not occur. E.g., if mating occurs in the ocean vs. on the beach.

Dominance correlates with reproductive success In Savanna baboons in Kenya there was a strong correlation between male dominance rank and the ability to monopolize fertile females across all groups studies.

Alternative mating tactics

Alternative male morphs in an isopod The isopod Paracerceis sculpta lives inside sponges in the Gulf of California. Males occur in three distinct morphs each with a different genotype. Each morph has equal fitness, and has different advantages in terms of mating. The alpha morph can physically fight off other males. But in a sponge with several females, an alpha male and a beta (female mimic) male, it is the female mimic who fathers the most offspring. Thus the advantage to female mimics increases if the alphas become more common. Natural selection results in the three morphs occurring at frequencies at which their fitness is equal. (fighter) (female mimic) (hider)

Alternative male tactics in lizards side-blotched lizard (Uta stansburiana)

Lizards play rock-scissors-paper

Alternative male tactics in scorpion flies Scorpion flies are not flies but insects in the order Mecoptera. The male genitalia vaguely look like a scorpion tail, hence the name. There is at least one common species in Belgium (Panorpa communis) which can often be seen in hedges and tall vegetation looking for prey.

Alternative male tactics in scorpion flies Alternative strategies: unequal fitness Scorpion flies (Panorpa): 10 males and 10 females in a cage Large males guard dead insects attractive to females; N=6 matings each Medium-sized males produce salivary gifts to attract females; N=2 matings each Small males force copulations on females N=1 mating each Males adopt different mating tactics depending upon size. The largest guard dead insects who are attractive to females. Smaller males use other tactics, such as producing nuptial gifts. But if the large males are removed smaller males will adopt the large male tactics. Faced with competition from larger males the smaller males adopt tactics which reflect their poor competitive ability. This is known as making the "best of a bad job".

Three male strategies Isopods equal fitness frequency dependent equilibrium Lizards not equal fitness; cyclical dynamics blue beats orange yellow beats blue orange beats yellow Scorpion flies not equal fitness; best of bad job strategy large male: guard insect medium male: salivary gift small male: forced copulation

Making the best of a bad job In the horseshoe crab males in good condition patrol the water off the beach and find and grasp females heading towards the shore to lay their eggs. Other males (satellite males) in bad condition swim onto the beach alone and crowd around paired couples to try to fertilise some eggs. Attached males fertilise 10 percent more eggs than satellite males, but satellite males still do better than if they would try to attach themselves to a female and be displaced by stronger males.

Coalition formation A significant number of subordinate baboon males are able to get access to estrous females by forming coalitions with other low-ranking males. Again, they are making the best of a bad job.

Iguana's Small, subordinate iguana males can win out from larger ones by ejaculating beforehand and keeping the sperm up to the brief moment they get a chance to mate, and before they are driven off by larger males.

Sperm competition

Sperm competition male-male competition can continue after sperm is released in both internally and externally fertilising species: sperm competition

Sperm competition in damselflies male male sperm transfer organ claspers female Calopteryx maculata: black-winged damselfly (N-America) Female may mate with several males. But male has a special penis that can draw out sperm from other males that mated with the female before, and this is 90-100% effective. But: female could choose to mate with yet another male.

Sperm competition in damselflies Calopteryx maculata: black-winged damselfly (N-America) Male penis has lateral horns which act as a brush and draw out sperm from other males.

Bean beetle males harm females Crudgington & Siva-Jothy Nature 2000 This photo shows the male’s penis. On copulation, the spines on the penis damage the female’s reproductive tract. The authors suggest that, if this damage is costly to the female (as is likely given that doubled-mated females died significantly sooner than single-mated females), then a damaged female is less likely to remate, thereby benefitting the damaging male. In addition, females kick the male during copulation and this shortens the mating. Females who have had their kicking legs removed mated for longer and had more genital damage than females who retained kicking legs. Bean beetle males harm females during insemination with a specially adapted spikey penis. This prevents the female from mating with another male.

Seminal toxins in the fruit fly Male injects female with toxin (protein ACp62F) Sedates female and prevents her from mating with other males But costly to female: shortens her lifespan Dorsal views of the ‘Swiss army knife’ gadgetry in the genitals of a male oriental cockroach, Blatta orientalis. Arnqvist3 has studied why such complex male genitals have evolved in insects, and he concludes that it is a result of sexual selection for genital devices that favour a fertilization bias for the mating male’s sperm over the stored sperm of the female’s previous mates. a, The genitals of male insects bear a huge number of intricate bits and pieces. The genitalic terms for orthopterans alone (crickets and allies) include phalli, epiprocts, paraprocts, cerci, gonotremes and even titillators (from the Latin titallo,‘tickle’). Chapman et al. Nature 1995

Seminal toxins in the fruit fly Holland & Rice: made a selection experiment. They bred males and females forcing them to be either monogamous or polygynous. The males from the monogamous lineage showed reduced expression of the seminal toxins and the females also partly lost their immunity to the toxin. Dorsal views of the ‘Swiss army knife’ gadgetry in the genitals of a male oriental cockroach, Blatta orientalis. Arnqvist3 has studied why such complex male genitals have evolved in insects, and he concludes that it is a result of sexual selection for genital devices that favour a fertilization bias for the mating male’s sperm over the stored sperm of the female’s previous mates. a, The genitals of male insects bear a huge number of intricate bits and pieces. The genitalic terms for orthopterans alone (crickets and allies) include phalli, epiprocts, paraprocts, cerci, gonotremes and even titillators (from the Latin titallo,‘tickle’).

Mate guarding

Mate guarding male damselfly graps the female in the tandem position so she cannot mate with another male male blueband goby accompanies female for his whole life

Mate guarding in the Seychelles warbler Clutch size = 1 egg; male guards fertile female; guarding ends when egg laid; fake egg can switch off male's guarding early. Seychelles warblers lay a single eggs. When this is laid the male need no longer guard his mate against rivals. By placing a fake eggs in the nest c. 4 days before the female laid the real egg, the experimenters were able to switch off guarding. The result is a massive increase in the number of intrusions, attempted an successful EPCs (extra pair copulations) by males.

Mate guarding in the Seychelles warbler Males adjust their mate guarding in relation to the risk of losing paternity to rivals. The more male neighbors around a breeding pair the more time male warblers spend guarding their partner.

Mate guarding in blue milkweed beetle Does time spent guarding your partner against other males give more offspring than abandoning her and looking for more mates? Janis Dickinson investigated this in the blue milkweed beetle. The male remains mounted on female's back for some time after copulation.

Mate guarding in blue milkweed beetle Dickinson removed male beetles from females. 25% of separated males found a new mate within 30 minutes. So guarding the female has a considerable cost in terms of missed mating opportunities. 50% of females found a new mate after guarding male was removed. So guarding the female has a considerable benefit in preventing the female from remating. Where do the costs and benefits balance out? By plugging these and other factors into a simple model it appears that guarding is beneficial if the last male fathers 40% or more of the female's offspring. Can you understand why this is so? If the last male fathers less offspring, then this means the female is less worth guarding (you were the last but probably not the only male to mate her), and if another male mates her he won't father many of her offspring anyway.

Mate guarding in blue milkweed beetle

4. Female choice

Female choice to obtain direct material benefits female choice most common several mechanisms, e.g. accepting sperm of males with large nuptial gifts rejecting sperm from low status males remating or not also: pollen incompatibility in plants - reject own pollen usually gives direct material benefits

Accepting sperm of males with large nuptial gifts: hanging scorpionflies Females copulate with a male for as long as they can keep on feeding on the nuptial gift. If this takes less than 5 minutes no sperm is transferred; 20 mins is required for complete transfer.

Remating or not in redback spiders Male transfers sperm and then commits suicide by jumping into the jaws of the female who then usually eats the male. This may seem maladaptive, but it is not: feeding the female by committing suicide reduces the chances that the female will mate with and dine on another male. Also, chances for a male to find another female are very slim because of intense predation. The selective pressure caused by females who may are may not remate has led to the evolution of male suicide.

Sperm ejection in Chickens Female chickens who have mated with a low status male are more likely to eject the sperm from their reproductive tract.

Sperm ejection in Dunnocks An interesting sort of sperm ejection occurs among Dunnocks, small brown birds common in English gardens. Alpha males try to prevent matings by lower-ranking males but are rarely successful. Most Dunnock matings are preceded by a ritual-like phenomenon called "cloaca-pecking." The female raises her tail exposing the cloaca. Instead of mating, the anticipating male pecks at the cloaca, an action that stimulates a pumping action and ejection of a droplet of sperm from previous matings. After the male inspects the droplet, normal mating follows. This bizarre scenario required the coordinated evolution of two different kinds of behavior (male and female) as well as the development of the female's sperm-ejection mechanism. Dunnocks (heggemus): male may peck at partner's cloaca if another male has been near her. In response she may eject a droplet of fluid containing sperm.

Female choice for males that provide more care Females of the fifteen-spined stickleback associate more with males that shake their bodies more frequently, which is a good indicator of how well they will be able to oxygenate the eggs later on.

Female choice for males that provide more care Sedge warbler (rietzanger): male song repertoire indicative of how good a father they will be later on. Females prefer to mate with males with a bigger song repertoire.

Female choice without direct material benefits previous examples: consistent with good parent theory but also in species without paternal care females often prefer distinct males, e.g. with brightly coloured plumage why?

Healthy mate theory: bowerbirds Male bowerbirds with high-quality bowers are less likely to carry ectoparasites in their feathers, so females that copulate with good bower builders will be less likely to pick up feather lice.

Good genes theory: sedge warblers Sedge warbler males: repertoire size is correlated with male heterozygosity. Females prefer males with a large repertoire and therefore also more outbred males. This increases the heterozygosity, and genetic quality, of the female's offspring.

Good genes theory: starlings Starlings (spreeuwen): males that sing at a higher rate have a stronger immune response measured by the swelling of a foreign chemical into their wings. Since females prefer males with high song rates they could be acquiring mates with strong immune systems, which will also be passed on to their offspring.

Good genes theory: Hamilton & Zuk hypothesis Hamilton & Zuk: in species subject to parasitic infection, individuals that can signal their relatively parasite-free state should be desirable males. They further argued that only high quality, parasite-free males would be able to produce costly, bright plumage displays (cf. Zahavian handicap). This would lead to plumage coloration being an honest signal of the male's ability to resist parasitic infections. Supportive evidence: correlation between plumage brightness and the incidence of blood parasites across a large sample of birds.

Good genes theory: peacock Male peacocks with larger eye-spots on their tails produce offspring that survive better when released from captivity.

Runaway selection theory Genes responsible for the male display have a pleiotropic effect when present in females and causes them to prefer males producing the display. Also has the advantage that the males that a female produces will also be preferred by females ("sexy sons"). Could work even if it causes females to prefer purely arbitrary characters with no survival advantage, or even a survival disadvantage. Russell Lande & Mark Kirkpatrick

Chase-away selection theory (preexisting bias) Lesson 2: The Evolution of Communication (Chapter 9 in Alcock) (exploitation) Brett Holland & Bill Rice

A preexisting sensory bias Male and female guppies eat Clusia fruits which are orange due to the presence of carotenoids. The same carotenoids also accumulate in males and lead to colourful patterns. Observation: females prefer colourful males. Why? Preexisting sensory bias for detecting orange fruits.