EEB 122: Principles of Evolution, Ecology and Behavior?

Lecture 13.?Sexual Selection

https://oyc.yale.edu/ecology-and-evolutionary-biology/eeb-122/lecture-13

Sexual selection is actually a component of natural selection. When Darwin?saw all of these extravagant behaviors and?extravagant?plumage?of the bird, he thought there must be something else going on, besides natural selection, and that's because Darwin thought that natural selection, in some sense, was the survival of the fittest.?We now know that natural selection really is the survival of those that reproduce the best, and that Sexual selection is a component of natural selection that is associated with mating success. So basically Sexual selection is a case in which mating success is trading off with survival.?

• The ratio of male to female mortality?in the United States?starts to diverge early in life, and by the time of late?teenage and early twenties, the ratio is climbing rather strikingly. This is from external and internal?causes.?And?this divergence?is enough to account for the different life spans of human males and females, which differ by about four or five years.?

• That is Sexual dimorphism, and Sexual dimorphism in mortality rates, and it appears to be associated with blockheaded risk-taking behavior. It appears that males behave differently at those ages than females do. Now we don't know whether that's evolved and genetic, or whether it's culturally influenced.

• From animal studies, the more polygynous the species, the shorter the male's lifespan relative to the female's.?There is not any difference in monogamous species.?If a change in a trait is going to increase lifetime reproductive success, by improving the ability of an individual to attract or to control a mate, or to achieve fertilization, it can be favored by selection, even if it lowers survival probability.?Sexual selection will change traits that influence mating success until the improvement in mating success is balanced by costs in other fitness components; then the response will stop.

• It?explains why organisms will take?extreme risks to mate and?why juveniles develop secondary Sexual characters only on maturation. That's because the secondary Sexual characters, which are the things that we think of as causing the two Sexes to look different in any species, bear with them costs, and those costs can be imposed from a variety of sources. The costs may be that if you look like an adult, you're going to elicit competitive behavior from other adults--you might get beaten up--or it may that it simply makes it much more difficult for you to escape a predator.?

The main questions about Sexual selection are how did it originate? There could not be any Sexual selection?before there was?anisogamy. There had to be gametes of different sizes, and there had to be individuals specialized on producing small ones and big ones before you could start getting things that functioned as males and females, and then evolve to begin to look like and behave like males and females.?

The mechanisms of Sexual selection are basically two: competing for mates and choosing mates. We are among the more Sexual primates,?not quite as Sexual as bonobos, but we are a relatively highly Sexed primate.?The strength of Sexual selection is actually on the day of mating determined by the operational Sex ratio; that is, the local ratio of males that are ready to mate with females who are ready to mate.?

• Competing and choosing have different consequences. It is the limiting Sex that can be choosey?and normally individuals of the other Sex compete. Now it is quite possible that if one Sex is limiting, and the other Sex is competing for the attentions of that Sex, that the individuals among the limited Sex can actually compete with each other for the attentions of the suitors. There's nothing ruling that out, yet?I'm describing here the processes and forces that are stronger in the two Sexes.

• Generally speaking, mate competition will be stronger in the Sex that has the greater reproductive potential, and it's the one that should be competing for the Sex with the lesser reproductive potential. And usually males have greater reproductive potential, females have lesser reproductive potential; so males compete and females choose.

• David Buss claims?that males choose young females that look healthy and have high reproductive potential, and females choose males that have access to resources and are likely to contribute to child rearing. ?And he says this is cross-cultural.?Obviously that could be controversial, and there are a lot of refinements on that picture, and there's a lot of evidence that could be better. That's for humans.

• There are some hypotheses for?animals. A female could decide,?"Does he control important resources? Will that one be a good parent? Will it supply food efficiently?" Or,?"Is that potential mate healthy? Is it free of parasites, and is it advertising its ability to resist parasites and pathogens with a costly signal that gives me an indication that in fact that thing is honest and is not trying to deceive me?" Or, "Does that potential mate have traits that are attractive to Sexual partners? Will I have a Sexy son?"

• This sets off a very interesting co-evolutionary process between the preference genes that are?expressed in the female's brain and the expression of that in the form of some kind of Sexy morphological trait in the male's morphology. And these genes for preference and genes for attraction come together in the offspring.

There is a Sexual selection maxim, which is kind of a default condition?that is eggs are expensive and sperm are cheap, so females are limiting and are going to be choosey, and males have potentially higher reproductive success over a lifetime than a female, but probably also higher variance in reproductive success.?The consequence of this is that the lifetime reproductive success of the females is basically limited by the number of offspring they can produce; the lifetime reproductive success of males, by the number of females they can fertilize. That's really asymmetrical.

• This is a case in which the Sex that is choosey changes in a plastic fashion as a function of how much food they have, and that's because in Katydids males contribute nourishment to the females in their spermatophores. So a female is not only getting sperm from a male, she's getting food from the male.

• If food is scarce, then female are actually reproductively limited by how many male spermatophores they can get. And at that point the females fight over the males and the males become choosey.

• When the food is abundant, the males are reproductively limited by the availability of females; females are getting a lot of food from sources other than spermatophores; males court and females are choosey.?

Now, what about competition for mates? There is a lot of armament out there in Nature.?There are major differences in body size of males and females in many species.?The evolution of that difference in body size is really driven by contests, scrambles and rivalries. The males'?fighting isn't ruling out female choice, it's making possible perhaps another kind of female choice. That does explain large, well-armed males, and the most striking examples of this dimorphism are in pinnipeds.?

• Bull elephant seals are very superior divers. They will go out offshore?100 miles or so, and dive down to a depth of oh between 1000 and 3000 feet, to fish for squid. A?male elephant seal will spend about nine months a year storing up food, because then he's going to haul up on a beach and try to protect a harem on the beach, and try to chase off other males and fight vigorously. And during that three months he doesn't eat.

• It is possible for these guys to control a harem of about forty or fifty female seals on the beach. They?are built for swimming sleekly through the water, chasing squid, not for humping along the beach with their four flippers.?But these guys do, for three months, and they get all beaten up, chasing off juvenile males that are coming in and trying to sneak copulations with their harems.

• Because of this spatial situation, juvenile males can?actually give the females a?chance to make another choice. So the juvenile males hang out sort of on the boundaries?between the harems of the big dominant males, and try to sneak copulations.

• An elephant seal will be about 1.6 times as long as a female, on the order of five or six times heavier than the female. That's a pretty strong relationship in biology, for Sexual dimorphism versus harem size, and that illustrates the importance of competition for mates in controlling the evolution of size differences between males and females.?

If you're really choosey and you're able to detect high quality territories or good genes or Sexy sons,?you can improve your fitness by being choosey. But remember to be choosey you have to take time.?If you shop too long, you may miss the opportunity because the shelf will be empty. ?So organisms should be careful, but not too careful. There's kind of an optimal waiting time, and as the season progresses, for a seasonally breeding organism, there's going to come a time when mating with anybody is better than not mating at all. So this business of being choosey is constrained by time.?

Now choice based on an immediate phenotypic benefit--that means I'm going to choose this mate because he's got a great territory and I'm going to get a lot of food, or I can see that my babies will have a lot of food--can explain a lot, but it won't explain extravagant male morphology or leks.

• Things that lek are peacocks, sage-grouse, Birds of Paradise.?Lek in Swedish has two meanings. Meaning number one is a sports place.

• It also means?in behavioral ecology?a traditional display ground where males come year after year to advertise and try to attract females to mate with them.

• It?is a mating systm in which the males are not going to?take care of the babies. The males sit there and display and fight with each other. Females come and mate with them, and the only thing that the female gets from the male is genes.?

What kind of an experiment could you do in the field to try to decide what's a female looking for? Malte Andersson worked on the African Widowbird. The males have naturally long tails, and they control territories within which two, three, four, five females might nest.?

• Malte shortened tails on some Widowbirds by simply cutting them off with scissors. On his control group he cut the tail off and glued it back together, so it didn't change in length. And then on his experimental group he cut the tail off--he took the cut tails from the short-tailed ones and glued them on to make super long tails.?So he had three groups. He had short-tailed controls and real long tails.

• The ones with shortened tails only averaged half a nest on their territory, and the ones with the lengthened tails averaged nearly two nests on their territory. Individuals were assigned at random to these different groups. And so the data indicate that female Widowbirds were building nests on territories of males with longer tails. And then the question is, if you're going to double your reproductive success with a longer tail,?why hasn't evolution done that to you?

• The answer is probably that natural selection is preventing a further increase in male tail length because females are preferring much longer tails than are found in natural populations.?

So?there's another hypothesis, and that is what is a female looking for? Well she's looking for an indication of good genes, under this hypothesis, and that would mean that a female should prefer a male displaying an honest costly signal?that they contain genes for superior survival ability; for example, genes for parasite and pathogen resistance, even for different MHC alleles.?The vertebrate immune system is partially integrated into the vertebrate nervous system. The two systems can send each other information. If there was a way that your sensory system could pick up information on the composition of the MHC alleles, in a potential partner, and send it to your brain, that would affect your mate choice.?

• There is an experiment about?body odor on how attractive a potential mate smells.?You?do the DNA sequencing to see whether or not the people who are reporting attractive or unattractive have similar or dissimilar MHC alleles, the ones that are reporting that a smell is attractive are the ones who have different immune genes, and the ones who are reporting that a smell is repugnant have similar immune genes.

• The way the immune system works in the offspring, to resist infectious disease, is by generating diversity within the body, and it can only do that if the genes are different. So you have to find a mate with different MHC alleles if you want to have disease resistant offspring.

• Where people make mistakes and they do mate with people who have similar MHC genes, they get into a situation where there are multiple spontaneous abortions. So it appears not only that there is a level of selection at mate choice, but there is also a level of rejection of zygotes that are potentially not going to resist infectious disease.

• If a male produced an ornament in order to advertise that he was resistant to disease, then you would expect that male fitness would decrease with increased parasite infection. So that would be an assumption behind it; that would be the selection that was driving it. The condition of his ornaments should decrease with increased parasite burden. So the less he was able to resist the parasites, the less dramatic an ornament he would be able to express. So that means that that ornament's got to be costly.

• Then there must be some heritable variation in resistance, or there wouldn't be any response to selection. Females should be choosing the most ornamented and the least parasitized males.

Now that would be a good genes argument. The male's got a gene for parasite resistance, so I'm going to make with him. And that is where the Fisherian process of Sexy sons would start. So I'm now shifting into the argument for the third hypothesis, which is you choose a male because you think that if you have a son by him, that son will get a lot of matings.?Preference for good genes will select for the preference itself, and that makes the preferred trait an object of selection, and it explains the evolution of ornamentation.?

• Suppose the reason a female guppy likes a male with an orange spot is that the only way he can make that orange spot is if he gets carotenoids out of the crustacea that he eats. So if he's really good at finding high quality food, he can make a bigger orange spot. So it's advertising his foraging ability.

• So that gene for foraging ability comes together in the offspring with the gene for the preference, and because the male has better foraging ability, the gene for the preference will hitchhike on the reproductive success of the gene for the foraging ability, and females will develop stronger and stronger preferences for a male with orange spots. It's thought that initially the preference develops because it's a preference for a gene that actually affects reproductive success in your offspring.

• What if now that guppy population moves into a new habitat that doesn't have any crustacean in it, and it becomes difficult perhaps for the males to make carotenoids? But they still can, they can still make orange spots. But the females have the preference. The male is no longer giving off a signal that's reliable in terms of good genes. All he is signaling is that he's attractive to females.?

Well now evolution has a new reason to maintain that selection. It's a selection simply for the attractiveness of the offspring, because a component of reproductive success is mating success, and by choosing a male that has an orange spot, the female is also choosing mating success in her sons.?

The female preference genes then hitchhike on the male's fitness genes and they get united in their offspring.?Once their preferences are established, they work on male traits that are otherwise neutral, or maybe even disadvantageous, except that they are preferred by females. So they lead to success in mating. Then mothers will gain in fitness by selecting fathers with heritable traits that make their sons attractive to females in the next generation.?In?some?cases, like stickleback,?the data in fact do not distinguish between the two hypotheses. It's not like it's either/or. Both things are going on at the same time. Females are choosing Sexy sons who are also parasite resistant.?

There is another hypothesis?that the sensory capacity inherited from ancestors would bias the traits. Females might just be selecting males they can see or hear especially well.?

• The?example is that the female eardrum in a Tungara frog is tuned to receive some frequencies better than others. The?male?can't change his call signal out of the frequency range that that female ear can hear. If she is attracted to him, he has reproductive success. But unfortunately, that's a perfectly fine frequency for a bat to hear. And in fact a fringe-lipped bat is a frog eating bat, and it does exceptionally well during frog breeding season by swooping in and munching up the males who are dutifully calling to try to attract their females.

• Now the idea here is that the male can't evolve out of a frequency range that the bat can hear because the female's eardrum is constrained to be a certain size; that's the sensory bias hypothesis.?

Now what is the actual context in which this is going on? Well it's when mating is happening, when choice is being made. And that's where the operational Sex ratio comes into play. It basically is determining the opportunity for selection, and it varies with mating system and parental care. So Sexual selection, which produces striking differences in the behavior and morphology of males and females, is correlated in ecology and evolution with mating systems and patterns of parental care.?

• In monogamy, equal numbers of males and females have offspring, and each Sex has one partner, and there's not very much difference in the operational Sex ratio and not much opportunity for Sexual selection.

• In polyandry there are more males than females, that have offspring, and each female has two or more male partners. So there is great variance in reproductive success among females; there's less variance in reproductive success among males.

• In the reverse pattern, in polygyny, more females than males have offspring, and each male has two or more female partners; that leads to harems and leks. And then there are things like polygynandry where each Sex may have several partners.

• Dunnocks,?a little brown bird,?are polygynandous. So each Sex is mating with several partners. A female sitting on a nest will have eggs in it that were inseminated by several males, and the father who's bringing food to that nest has his genes in eggs that are in several other nests.

So to summarize Sexual selection. It's a component of natural selection in which mating success trades off with survival. It's not a separate kind of selection, it's part of natural selection. It accounts for many of the attractive ornaments of plants and animals. It raises the interesting issue of aesthetics and why our brains see things as beautiful that other things find attractive.?

There is contest competition for mates which are the scarcer reproductive resource, and that will explain a lot of Sexual size dimorphism--bull elephant seals, things like that--particularly in polygenous species. We've seen there that the degree of dimorphism is directly related to the degree of polygamy; the bigger the harem, the bigger the size dimorphism.?

And whether or not this indirect mechanism--this Fisherian runaway process, that leads to preference for Sexy sons--whether that is really needed to explain ornaments in lekking species, it seems to be logically the only possible explanation left standing.?