EEB 122: Principles of Evolution, Ecology and Behavior?

Lecture 35. Alternative Breeding Strategies

https://oyc.yale.edu/ecology-and-evolutionary-biology/eeb-122/lecture-35

Today we're going to talk about alternative breeding strategies.?The whole issue of having an alternative breeding strategy revolves around frequency dependence.?So the usual scenario is that at some point in the evolutionary past a male has achieved a dominant mating status, and that sexual selection has then driven the evolution of his behavior and his morphology--the mating system, polygeny, polyandry, whatever; in which case it would be a female who would achieve the dominant mating status--so that there was a focal pair, and that that biology got pushed to a certain degree.?

• It?often happens in various kinds of frogs, not just bullfrogs, that the male calls, the female hears the male calling, moves toward the pond, and the male will then grasp the female with incredibly strong forearms.?Once they get onto a female it's actually extremely hard to pry them off.?If they can stay locked onto her when she releases her eggs, they will get the babies.?If a small male gets onto the female first, the large male will grab both of them and practically squeeze the small male to death.

• If it weren't the case that the pond was only going to be there for a little while, and only really suitable for raising baby?frogs for a little while, it wouldn't be so intense.?It all happens in a period of about twenty-four to forty-eight hours.?Now the point of this is that the behavior of the dominant male, and the female who's attracted to him, created the opportunity for the alternative behavior of the small male.

Now a similar kind of alternative--well similar in the abstract sense; a similar alternative mating strategy has evolved in figs and fig wasps. And figs and fig wasps are one of the wonders of ecology and evolution.?

• There are more than 500 species of figs in the world--many of them in tropical rainforests; many of them critical ecological resources providing food throughout seasons when other trees are not providing food--and each one of these species of figs, in general, has its own fig wasp, and if it didn't have that fig wasp, it couldn't get pollinated.

• The figs are sacrificing some of their own seeds to raise the wasps that pollinate them. And this clearly has evolved from an ancestral situation in which the wasps were actually parasitizing the figs, and ripping them off, but now has evolved into a very complicated mutualistic relationship.

• The strategies of both the figs and the wasps vary. Sometimes the figs are monoecious, sometimes they're diecious; in other words, sometimes they are producing fruits that only have male flowers or only have female flowers, and sometimes they're producing fruits that have both kinds of flowers in the same fruit. And the wasps have really highly differentiated strategies that depend on whether they're copulating inside the fig, or?outside the fig,?and sometimes you get both kinds of strategies in the same species of wasp.?

The figs can make either long or short styled flowers. And what that means is that they are making flowers which are going to be targeted by fig wasps, or not targeted by fig wasps, for their babies.?

• The figs that have long styled flowers are going to be getting pollinated, and there aren't going to be any larvae developing on them. These are the ones that are going to make new figs. And the figs that make short styled flowers are going to be chosen--in this species of fig; this isn't for all, but this is for one of the 600 species of figs--they will be chosen by the wasp that will oviposit in them, and the wasps will eclose.

• They will mate; in many cases they will mate inside the fig, and then when the females leave the fig, the timing of the fig's flower maturation is such that as the females force their way out of a narrow aperture, there are flowers bearing pollen right next to that aperture on the inside, and the female takes them out, and then she flies off to oviposit in another fig, which is how the pollination is achieved.

• So they had to set up two separate ways of making seeds; the ones that the wasps would use and the ones that would make future figs. Other fig species have partitioned this in other ways. So there's an interesting complexity of evolution that's gone on in this relationship.?

Now the alternative mating strategies are that there will be fighting males or dispersing males. There is a frequency dependent thing going on inside one of those figs, as the males are hatching out. If they fight with each other and kill each other, then the survivor will be the only male who is in that fig, or one of the few males in that fig, who can mate with the females that are coming out.?

• If you commit to that strategy, you are committing to an extremely aggressive, live by the sword die by the sword, kind of existence, and it all gets carried out in a dark little fig, and you're just waiting for the first female to hatch out so that you can mate with her, and you get as many as you can, and then you never fly, because you don't have any wings. You die in the fig. So that's your protein intake; it's dead males.

• On the other hand a certain number of the females are going to manage to get out of the fig without being mated inside, and if you can go out and find them?outside, then you don't have to commit to fighting. However, there are very strong morphological tradeoffs between the two kinds of things. You can't do both well; so you're committing to doing one or the other well.

• And how much each pays depends on the local biology. How likely is it that the female will be able to get out of a seed, an eclose, and get her wings ready to go, and get out of there before one of these fighting males comes over and gets her??So that's what creates the frequency dependence.?

And you can see these things are radically morphologically different from one another. This is a case in which the alternative reproductive tactics are really resulting in changes that you could just pick up by looking at the things. These guys are down about one millimeter long nut it has resulted in major morphological change.?

And, by the way, these, from an evo-devo perspective, this is neat because all of these forms are elicited essentially from the same genotype. These guys are haploid; these are the males. This is the female; she's diploid. Otherwise they have the same genotype, and these alternatives here are probably being determined just by one autosomal locus with two alleles, that are determining whether or not you are a type that flies out of the nest or stays in the nest and fights. And you can see that the female is equipped with really a beautiful, exquisitely long ovipositor to get her egg into the fig seed.?

The bullfrog biology is relatively straightforward; the fig wasp biology is almost arbitrarily complex. But they both create situations in which alternative male mating tactics are possible. And the thing that drives that is that there is a very well developed, evolved, prior biology, that means an alternative has an opportunity to insinuate itself. You can think of the alternatives as being parasites on the prior condition.?

Now, there is probably no group of organisms in which the diversity of mating tactics and parental styles has been more broadly and diversely developed than in fish.?There are three different kinds of parasitic male reproductive behaviors.?

• The sneakers are using speed or stealth to get access to a spawning. So they don't necessarily look like a female. They just kind of hang back, let the spawning start, and then they whip in.

• The female mimics actually deceive the territorial or guarding males into thinking that they are something to mate with, and then a female comes in and when she spawns the female mimics then reveal their true colors and release sperm, rather than eggs.

• The pirate males are males that steal fertilization by being big bullies. So they let some other guy do all the work of cleaning a territory and setting up a nest and going through all of the trouble of displaying and attracting a female, and then just as she arrives they whip in, and because they're bigger and tougher they push him out. So that's a pirate.

• There are also cooperative male reproductive behaviors. Satellite males can display and can contribute to territorial defense and parental care. And so we don't have to view this as strictly a short-term, selfish kind of exploitation. There can be cooperative mating going on, and it will stabilize if it's really win-win, so that everybody in it is winning something from the interaction.?

If you just look at these morphologies, the satellites, the sneakers and the mimics are usually lacking sexually selected ornaments, and the guards and the pirates usually have such ornaments.?So the pirates kind of look like the guards.They're not so much morphologically differentiated as they are behaviorally differentiated.?Some of cyprinids?have alternative tactics. Some gobies have alternative tactics. The wrasses here are in the Labridae. But there are some alternative reproductive tactics in the cichlids and so forth.?

• The take-home point from that picture is hey, fish do a lot of different things, and they have independently converged on alternative male reproductive tactics multiple times; which you can see from the fact that the black is spottily distributed across the phylogenetic tree.

• If you go through that tree, we?assume that we're usually starting from mate monopolization; so a guarding male and one female. It looks like out of that ancestral state there has been some evolution of group spawning, and there's been some transition from that back through mate monopolization. There seems to have been some move from group spawning directly over to alternative reproductive tactics.

• If we look at?alternative reproductive tactics, it looks like the most frequent one is that sneakers pop up. That seems to be the easiest, at least the most frequent evolutionary transition. And from sneakers, or from mate monopolization, you can get female mimics; you can get satellite males. So this is the cooperative one. And then the pirates are not so common.?

This is a wrasse that lives in the Mediterranean.?It is a case in which the nesting males are providing parental care, and they are?guarding males.?They are the ones that build the nest. There are smaller non-nesting males that come in and sneak spawns. A nest takes about ten days.?About one-third of all nests are deserted, and they can be deserted either because there's an intra-specific or an inter-specific interaction. And it is the females that choose spawning situations. They're not really choosing males or territories; they're choosing to go into a situation in which they see one male, many males, a certain kind of general topography.

It's a cost-benefit analysis using?evolutionary game theory--should you guard or should you sneak? In other words, should you invest your energy in guarding your nest and in guarding your female, or should you try to increase your sperm production??So that's the basic assumption. Either it's guarding or it's sperm production.?

• If you guard, one assumes that's decreasing the risk of sperm competition. If you do get into the sperm production racket, then it's thought to be a fair lottery, which means that the probability of a fertilization is just directly proportional to what frequency your sperm are in the pool of sperm that's being produced. And these fish have external fertilization, so you can pretty much estimate that by analyzing a sample of a cloud of sperm produced at a spawning.

• The guarding males don't know if they're in sperm competition, because the female mimics look like females. So the male is guarding and he thinks he may have a number of females around him, and it's hard for him to know whether they're females or not. That's not true of the female mimics; they know that they're going to be in sperm competition.?

So this just gives you an example of how a behavioral ecologist would think about that problem. You do a Cartesian reduction, you break it down into its elements, and you write down what would be your reproductive success if you were guarding mates.?

• If you're a guarder, and you're considering the allocation within your own body to these two possibilities, you just ask, "When am I going to get more out of guarding than I am going to get out of sperm production?" And that simplifies to this; which is that the relative cost of mate guarding has got to be smaller than the relative cost of sperm production.

• The nesting males don't know if they'll be in sperm competition. The female mimics know they're always going to be in sperm competition. And the fertilization rates are about 100%. So the nesting males are able to reduce their risk of sperm competition through mate guarding.?And the proportion of spawns which are actually successfully snuck does increase with the number of mimicking males at the nest.

• This is sperm competition. If a pair is spawning, the male has produced relatively little sperm, and if there are sneakers that are going in--so this is a pair plus one sneaker--this is the additional amount of sperm that he is putting into the spawning. So he has obviously taken advantage of the fact that he doesn't have to put energy into guarding, and he has allocated that into spawning.

• However, because of the behavior and the dominance of the guarding male, who is larger, he is usually able to get closer to the female, and in fact he is actually getting more offspring out of his 1.5 million sperm than the sneaker is out of his approximately 5 million sperm.

• So these males are actually getting well paid by investing in guarding, rather than allocating the sperm. And the model is predicting that mate guarding should lead to higher success.

• So the sneakers are essentially males that are making?the best of a bad job, and they suffer from high variance in mating success. So they try, and they go from one male to another, and they try repeatedly over the course of the season. And the percentage of eggs they're able to fertilize is going up and down a lot with each spawning; whereas the guarding males are getting less variance and a better geometric mean of total eggs fertilized throughout the spawning season.?

I think that it's the basic view of the world that comes out of almost every analysis of frequency dependence using game theory. It is a world in which there isn't an optimal solution. It's a world in which there are losers. It's a world in which there is conflict.?And certainly this is a mating system in which long-term conflict is always going to be there, and it's basically because the more guarders there are, the more opportunities there are for sneakers; and the more sneakers there are, the lower the mating success of sneakers is going to be. So they will always be maintained at intermediate frequency and they'll never go away.?

Now one of the interesting parts of behavioral ecology that has received a lot of emphasis in the last?twenty years is the behavioral ecology of gametes. So we consider the alternative tactics of sperm, or the alternative tactics of eggs, and can we actually see alternative tactics reflected at the level of the sperm, as well as the level of the adult??

• The sperm that are produced by males that are adopting different tactics actually have different swimming speeds. So the open circles are pirates; the boxes are territorial males; the sneakers are these filled dots; and the triangles are satellite males.

• And this is a cichlid fish from Lake Tanganyika that broods in shells, and has this range of alternative male behaviors. And if you look at how fast the sperm can swim, they have, in the first minute, they all have better swimming speeds than after about a minute or so. So what happens is they go through their energy stores really quickly--it's like that first minute is really important, so they all sprint for a minute--but then the sneakers manage to hang on better over the next five or six minutes.

• So this is an interesting case where the whole organism, alternative morphology and behavior, is associated with a syndrome at the gamete level of changes in swimming speed. This hasn't been much investigated, and my guess is that there's a lot more stuff like this going on than we already know about.

How about other fish? Well a lot of the things that you're probably familiar with happen to be species in which alternative male reproductive tactics are well described. One of the classic ones is the bluegill sunfish, and another are the West Coast salmon.?

• The bluegill is a fairly long-lived sunfish, and the female is born and matures at about four years, and then has probably about another three to four years of reproductive life.?The male makes a decision after late in its first year?either to become a sneaker and a female mimic, or to commit to growing for another five years before it will mature into the dominant guarding male form.

• The bluegills,?like?most centrarchids, dig a nest and deposit- and the male is going to be guarding eggs that are deposited there. And the sneaker will come in and basically come into a breeding assemblage, and actually get in between the male and the female, while the eggs and sperms are being released. He actually pushes in between them, he's sandwiched in between them when he releases his own sperm.

• In West Coast salmon, which are genus?Oncorhynchus, Pacific salmon, the difference in size is even more dramatic, and the difference in life history is huge. So again in the summer following?the first birthday, the male is making a decision either to stay at home in the stream, or go to sea. Salmon are anadromous they run up streams to spawn. They lay their eggs into well aerated gravel reds in the spring, in the stream. When they hatch out, depending on the species, they either spend a little time or a lot of time in fresh water.

• Many of them go to sea. And what they get by going to sea--which by the way is a very risky thing to do; it's dangerous; you run a gauntlet of predators going downstream; you get out into the North Pacific and you have to deal with seals and killer whales and all kinds of things that want to eat you while you're growing up.

• What you get for that is rapid growth. You can eat all kinds of stuff in the ocean that's not available in fresh water. So you take a huge mortality risk to get the benefit of growing large. Then when you come back, the female will basically make a nest in the stream.

The eggs are released and they fall down into the gravel, and actually the insemination is going to go on down in the gravel. So it's not as though this is something that's easy to control. Doubtless, if you are an adult ocean going male, you are a bit irritated to have these little whippersnappers there stealing your matings from you. But they're so small that they can actually go down and hide in the gravel.?

So, in fact, it's a stable polymorphism. Both--the female would never actually release her eggs if there weren't a big guarding male there. These little guys just don't elicit that kind of reaction from her. So his presence is creating this opportunity for them.?

Now it turns out that there are sneakers and guarders also in dung beetles. If you look across sixteen different species of dung beetles, that have sneakers, you can document that the sneakers have larger testes, and that sneaker frequency actually influenced male expenditure on ejaculate.?So this is a case in which the guarding males can see that there's a sneaker there, and if there is a sneaker there, they up the amount that they put into the ejaculate. So there is a flexible local response that's triggered by this.?

In what kind of a mating system do you think you might have the potential for the evolution of an alternative female reproductive strategy? In?polyandry. This is a pair; this is a male and a female jacana. She's got about four or five of these guys, that she's guarding.?

So she has a territory that's about an acre, on which four or five males are sitting on eggs, and she is defending all of them. And you can see that her fighting spurs here on her wings are a bit larger than the male's, and she takes the lead in defense.?

In this kind of a situation you might think that an alternative female reproductive tactic could evolve. In fact, polyandry is so rare in the animal world that there's very little evidence for it. But certainly abstractly that's the sort of situation in which it could occur. The other naturally is more cultural. That would be in the harems of the great dynasties; lots of alternative female reproductive tactics there.?

• So the main issues that we see in alternative breeding strategies are first this idea of frequency dependence. It's that once you get a guarding male and a female well evolved, they then form a focus for further evolution that creates the opportunity for a frequency dependent minority behavior, like sneaking or pirates or female mimics.?The condition dependence of this is well established.?

• With the fish that it's in the late summer, right after their first birthday, that they're making a decision to go one way or another. That decision, whether you're going to grow up, develop into a guarder or into a sneaker or a female mimic, is often determined by your condition at that point. Have you been able to grow fast or are you growing slowly? And if you are at the upper end of your growth cohort, if you're one of the really good growers, you probably commit, if you're a salmon, to going to sea; if you are a bluegill sunfish to growing up, spending another five years to become a guarder; and if you're at the lower end of that, you will commit to becoming a female mimic or a sneaker.

• And it's important to see that that's a condition-dependent strategy, and it can depend on a lot of things. It doesn't necessarily depend just on the genetic quality of that particular individual; it can depend on the growth history, the local environment, anything that's going to lead to either a rapid or a slow growth curve.?

Female choice is often an open issue. You might think that females might want to favor one or the other of two male morphs, but in fact there may not be much reason for female choice. You're a female. You've got thousands of years of evolutionary history to inform your decisions. You see the guarder and the sneaker. Should you prefer one? what happens in the frequency dependence of the two??

• Let's suppose they're at evolutionary equilibrium.?What's the relative fitness? They'll be equal. So if you're looking at two guys that actually because of the frequency dependent process have come to an evolutionary equilibrium, and you're scratching your head and trying to decide, should I make a choice between them? The answer is evolution doesn't care. Those guys are going to give you the same number of grandchildren. There isn't any reason for the females to prefer one over the other. They're going to get the same number of grandchildren out of both.

• The females?have an evolutionary history of having started out in that situation, and so the lack of female preference is probably more that they're not chasing away the sneakers. And they do?want to get their eggs into a nest. And only the guarder is going to do that for them. So in that sense they have to prefer the guarder because he'll take care of their eggs.

• But when they're actually in the mating situation, and they have the option of going five inches to the left or five inches to the right, and they can see that they're surrounded by a guarder and a bunch of sneakers, they don't--in that situation they don't care. Because their eggs are going to get into that guarder's nests, whether they're fertilized by the guarder or by the sneaker.?