Principles of Evolution, Ecology and Behavior

E&EB 122 - Lecture 34 - Mating Systems and Parental Care

Chapter 1. Introduction [00:00:00]

Professor Stephen Stearns: Today we're going to talk about mating systems and the way that they interact with parental care, and a bit about parental neglect, as well as parental care, and parental conflict over care. So there was just a little hint of that in the elephant example. What kind of a mating system do elephants have? Anybody know?

Student: Harem.

Professor Stephen Stearns: It's a harem, it's a harem. Actually it's a family structured situation. Normally there is a matriarch who is a grandmother, and then her daughters are there. The bulls come in during breeding season, and normally the males are separated from the females.

Anybody know about how far away one elephant can hear another elephant? It's thought to be on the order of ten to fifteen kilometers. They communicate like blue whales, with extremely low, intense low-frequency rumbling sounds. So, in fact, they can find each other from a long distance. So even though a bull elephant might be ten or fifteen kilometers away from a matriarch and her group of potential mates, he can get there in a hurry; he knows where they are.

Okay, so today we're going to talk about benefits and costs of parental care. We're going to note that the degree of parental care varies tremendously among different species of organisms. We'll see that there are interesting reasons why females, in some cases, and males in others, and in only a few cases both parents, care for the offspring. We'll consider the issue of when it pays a parent to neglect or kill an offspring, or when it pays offspring to kill siblings.

And a lot of these kinds of questions have been illuminated by the thought of Tim Clutton-Brock. Here is Tim on his ranch at the border between South Africa and Botswana, with his group of habituated meerkats. And Tim has got an interesting way of thinking that I recommend you look into. He likes to come up with extremely simple explanations as alternatives for current bandwagons.

So Tim has published a number of papers in which he offers simple explanations for things that people thought had been selected by kin selection; simple explanations for cooperation or living in a group and things like that. And in so doing he is actually expressing what one might call the empiricist Cambridge tradition, as opposed to the theoretical Oxford tradition.

The word that the Cambridge people have for Oxford is the art school in the midlands, and that the Oxford people have for Cambridge is the technical school in the downs. So they differ in their--they differ in interesting ways. At any rate, that's Tim on his ranch in South Africa.

He's worried a lot about parental care, and he's written a whole book about it. So parental care is anything that the parent does that increases the fitness of that particular parent's offspring. And investment is different from care.

Parental investment, which really was defined by Robert Trivers, is the extent to which parental care reduces the parent's residual reproductive value. So it's basically measured by looking at the reduction in residual reproductive value. So it's something that increases the fitness of this offspring, or this set of offspring, at a cost to any other component of the parent's future fitness. Okay?

Chapter 2. Different Types of Parental Care and Investment [00:03:58]

So how do they do it? Well there are lots of ways. They can prepare nests, produce gametes, take care of eggs. There's care of young; without getting them any food, you can just protect them from predators. You can provision young before hatching or birth. There are lots of ways of doing this. You can store food; we'll see examples of that.

You can allow the offspring to eat you; which is what spiders do, and some mites. You can set up a situation in which offspring are eating eggs or siblings; that's adelphophagy, so that's kind of an elaborate way of providing a supermarket for your offspring. You can have them eat special secretions of ovary or oviduct, and we'll see an interesting example of that. They can eat secretions produced in special brood chambers, or they can get nourished via placentas or pseudo-placentas.

So we ourselves are extremely derived in the way that we provide parental care. And if we look at Nature, we see a huge range of variation. And we can see cases in which evolution has taken parental care to a certain point and then stopped--like this seems to be good enough, or maybe this is the best--and it's not the situation we have.

So here's some data that addresses a pretty straightforward question. These are the first, second and third eggs, which are laid into a herring gull nest, and what you can see basically is that the heavier the egg, the higher the survival or the lower the mortality.

So if the egg is heavy--and it doesn't really matter whether it's the first, second or third in the series--then the probability of fledging is going to be about 80%, and if the egg is small, the probability of death is going to be just about 100%.

So this is a herring gull chick, hatching out of an egg. And what you can see from that simple data is that making bigger eggs is better for herring gulls, and it makes a big difference to their abilities probably to themoregulate, resist disease, resist tics and parasites; all sorts of stuff.

Now in terms of paternal care--this is a frog, the Coquí frog from Puerto Rico. And it has, by the way, spread around the world and is something of a pest, because if you hear a couple of thousand frogs going "coquí, coquí, coquí" all night, you don't sleep very well. So people in Coquí infested areas are sleep deprived, and they don't like it.

But it's an interesting frog because it has male parental care, and the frogs, the male frogs, are tending a bunch of tadpoles that are living in the water which is resting between the leaf of a plant and the main stem of the plant. So they're up in a tree, and they're guarding this from snakes, insect predators, other kinds of things. And if you remove the male at various stages of egg development--this graphs what percent of the eggs are going to hatch and turn into tadpoles.

And basically you can see--and by the way, these are about one to two days for each stage of development; so it's roughly three to four weeks that's going on here--you can see that if the eggs have been allowed to develop quite a while, then removing the father doesn't make that much difference; after the sixteenth stage they're going to make it. But early in the process his presence is absolutely critical. So there really isn't any way that this father can abandon that nest without suffering a huge fitness loss; and that's measured by these low numbers down here.

It can be quite risky to guard a nest. So this is a fish with a great name; it's called the lump-sucker, and it lives off of Scotland, and it lives in places off of Scotland where there are otters that are foraging in the shallow water near shore. And the males are guarding nests.

This is, by the way, not an unusual mating pattern in fish. You have it in gobies, you have it in sticklebacks. Males--in some wrasses--you'll have a male build a nest and females will come and deposit eggs in it, and the male will guard the eggs.

And basically what this shows is the number of lump-suckers that are caught by otters, and you can see that the males, who are defending the nest, have a much higher probability of getting killed by an otter than the females. So this is something where parental care really has a high cost. Defending the offspring can involve death.

Now guarding the offspring is not necessarily something that involves provisioning the offspring. Here is a Cacao stinkbug in Trinidad, and you can see that it is huddled over--it's a female--and it's huddled over all of these offspring that have hatched out of these eggs, and they will guard the eggs and the nymphs, and if you pull the mother off, there probably won't be any eggs that survive to produce nymphs.

And these things will get nailed, the babies will get nailed by parasitoid wasps; they will get nailed by foraging lacewings. There is a very diverse and fascinating group of predators and parasitoids that will do things like eat insect eggs. And here is a nice photo of an Australian stinkbug with all of its offspring huddled underneath it.

Parental care is actually fairly widespread in the insects and in other arthropods. Centipedes are among the really great parents of the world. They are nasty and they will sting you, but they have a nest and they go out foraging and bring food back to their babies. And centipedes will raise their babies until they are virtually the size of the adults. So they actually get weaned at about 80% adult size. They have usually a clutch of perhaps ten or twelve offspring.

So here is an example where the provisioning is done before the eggs hatch or are born. This is something that a scarab beetle does. And there are a number of beetles--the dung beetles, the burying beetles and the scarab beetles--that will dig tunnels into the ground, put food into the tunnels, and then the female will lay her egg on the food.

So often one of the choice criteria for the female is how good is my male at digging a tunnel, and is he actively engaged in provisioning it? So the male clears the entrance. He's going to defend it. Males gather fresh leaves and bugs. He takes them down to the female. She makes them into elliptical balls, and then lays her egg here, into something that develops into a grub, and then eats up the balls and pupates down in the hole.

Some of the more ghastly kinds of parental care involve setting up a situation in which siblings eat each other. And the eating of a sibling has a nice Greek name, which makes it a little bit more clinical, so you don't get so emotionally involved with it, adelphophagy; okay, the eating of siblings.

And it is not uncommon in sharks. This is an early dissection of a pregnancy in a porbeagle shark; and you see here an offspring that has a big yolk sack and it's starting to grow. And normally a porbeagle shark will start out with a fair number of embryos; something on the order of ten to twenty. And often only one of them survives to be born; it's the one that managed to eat up all the others.

And an adult porbeagle shark is a pretty impressive object. This is actually not a really big one; okay, this is--it's about six feet long. Porbeagle sharks will get up to about twelve or fifteen feet long. And other sharks that do this include bull sharks in the rivers of Central--you can catch them in the rivers of Central America--and several other shark species.

You can also find this kind of behavior in Whelks. So there are mollusks that will lay eggs in clumps, and the first one to hatch out goes around and eats the others. So it's a method of ensuring that there is a high quality, appropriately balanced diet awaiting your offspring.

These things that they're eating have got exactly the biochemical constituents that you need. And it's an interesting theoretical issue to think of how can the payoff in the quality of the one offspring possibly compensate for the loss in numbers of the say ten or fifteen that died in nourishing it?

Now another way to nourish young is to have some kind of specialized secretion in the ovary or the oviduct, and that's the case in a vector of great medical importance, Glossina, the tsetse fly. And it has a really very interesting life history. It just gives birth to one offspring at a time. Most flies will go around laying, you know, fifteen, twenty, fifty eggs a day, something like that. Glossina just makes them one at a time, and they make them big and lunky and high quality.

And it stays in the mother's reproductive system until its second instar, and it's getting fed with a milky secretion there that it's absorbing through its mouth. When it's born--here it's being born--it immediately then falls into the soil, digs into the soil and pupates. So it doesn't feed at all outside the mother. The mother has given it everything it's going to get.

Other things that feed offspring with secretions in brood chambers are pipefish and seahorses; and there are some frogs that will do this. And some of these have kind of pseudo-placenta where there are blood vessels that surround the brood chamber.

And in the case, of course, of the seahorse, the female has an ovipositor that looks kind of like a phallus. So when seahorses copulate, the female takes her ovipositor and inserts it into a slit in the male's brood pouch, and deposits the babies into the male's brood pouch; which is an interesting issue. And, of course, seahorses have lots of other wonderful things. The leafy sea-dragon, by the way, which is a favorite of aquariums and book covers, lives off the coast of South Australia; so it actually is a fairly coldwater seahorse.

Then you can take care of your babies, not by giving them something before they're born, but you can make a nice egg, and then when it hatches you can feed them after they're born. And that is something which is done by burying beetles. So we have burying beetles to thank for the fact that the landscape is not littered with corpses.

I have been fairly impressed--I have to trap mice out of my house sometimes; I have both white-footed deer mice and Southern bog lemmings in my house in Hamden. And my method of disposal is pretty straightforward. I take them out of the trap and I throw them in the garden. They're gone in the summertime within one night. The burying beetles come along and take care of them.

Chapter 3. Relationships between Mating Systems and Parental Care [00:17:25]

So that was a bit of the natural history. Okay? Now are there overall connections? Are there general patterns that we can pull out for parental care? Well there is, as you might think, as would be logical, there is a relationship between the mating system and the pattern of parental care. So if both parents care for the offspring, then they are usually either monogamous in their mating system--so things like swans--or they're polygynandrous, which means that they're things like dunnocks. If only the female takes care, that's usually a polygenous species. So the only thing that the male is providing is display behavior and sperm, and then the female is on her own with the offspring.

The ones that are male-only are either polyandrous or polygynandrous. Male-only parental care therefore usually turns up in the few polyandrous bird species, or in things like ostriches, which are not really polyandrous but where they have a male that will protect a large clutch of eggs, into which many females will deposit eggs; and the fish that have the same kind of pattern. Okay? So sticklebacks, lump-suckers, gobies, things like that.

The issue of--you can think of it like this. Who gets stuck with the kids? And the type of fertilization really has quite a bit to do with the probability that it will be the male or the female that is going to do the parental care and raise the offspring. Species that have external fertilization are more likely to have male parental care than species with internal fertilization. And that makes sense because with external fertilization the female is coming and spawning with the male, and the object to be cared for is then actually physically there in a space that the male might have reasons to want to defend.

In internal fertilization, the offspring are actually contained in and physically inside of the female, and they're going to be there for a while, which gives the male opportunity to wander off, or run off. And so the type of fertilization, for very simple reasons, is associated with whether the male or the female takes care of the babies.

So one of the reasons that seahorses are really a striking an exception to almost everything is that they're monogamous and they have internal fertilization, but they have male parental care. So they are monogamous. They will stay together as a pair, throughout their lives.

They have internal fertilization inside the male's brood pouch, but it is the male, of course, who's taking care of them. And the reason is the same: basically they're in his brood pouch and the female can wander off. In this case it's interesting; she doesn't really, she sticks around.

So here are some examples. The swans, which are monogamous, and then the dunnocks, which are polygyandrous, are cases where both parents will care for the offspring. If you want to see swans nesting right now, just go out Whitney, turn left on Waite, go down across Lake Whitney, and you can see three swan nests that have been constructed in the last few days. There will be cygnets within a few weeks. So maybe before you leave for the summer, if you have a break, go out to Lake Whitney and you will see baby swans.

The ones where the mother takes care of the offspring are usually harem-based. Now the reasons for the existence of the harems are different in things like elk and deer and in marmotes. With elk and deer, they are foraging widely, and the females are in a group for protection against predators. And the males, of course, have a mating season and fight with each other for access to the females. But they're moving around. And the male, during mating season, will defend a harem. So this will happen, of course, also with things like elephant seals, where you have harem defense. But it's a special case with a broad-leaf foraging ungulate.

With something like a marmote, the harem is basically based--it's a resource defense harem where the male is sitting on a pile of rocks, and he's defending his pile of rocks against other males. And the females live in the pile of rocks, and they would live in that pile of rocks if the male was there or not; I mean, they use that as their refuge. So basically what he does is he finds a place in the environment that the females need, and then he defends it against other males.

So that is a resource-based kind of harem mechanism. Whereas here it's not the resources, it's just the females themselves that are getting defended by the males. The females are wandering all around looking for food.

The ones where it's the father only are things like phalaropes, which are a genus of sandpipers that nest in the North and into the Arctic. This is the brightly colored female phalarope, and in related species of sandpipers that are not polyandrous, the bright color and the secondary sexual characteristics are in the male, not in the female.

And when the female is developing her bright colors and displaying to the male, her ovaries are secreting testosterone, and she defends the territory and goes around and lays eggs in three or four nests. And when the males are sitting on the eggs that she has put in the nest, their testes are producing estrogen.

So, in fact, the switch in sex role is handled by a hormonal switch, and it's eliciting a genetic program that is evidently present in both sexes and can either feminize or androgenize the bird in which the hormones are produced. And that's how the switch in mating system is handled.

Pipefish and their relatives, the seahorses, are also cases that have male parental care. And in the seahorse that's probably a case where there was a prior period of polyandry; like pipefishes or like phalaropes, where you had one female mating with several males, and then that developed into monogamy. Okay?

So how could that happen? How could you possibly get into polyandry and then possibly from that go into monogamy? Well having one female mating with several males might occur when one parent can rear as many offspring as two, when the foraging is good. So, you know, from the female's point of view, sticking this male with three or four eggs, and then going off and finding another male and giving him three or four eggs will be much more likely to evolve when that act of going to the second male doesn't harm the fitness prospects of the first brood so much. So the father really could take care of that many.

It's only likely to happen if you're starting from a position where the males are already pretty heavily involved; you know, you can't make a huge jump into this kind of mating system, you have to be evolving from a mating system in which both parents are already taking care of the offspring.

It probably happens mainly where therefore where the clutches are small, and you can produce eggs pretty rapidly. And this seems to be true in things like the phalaropes, polyandrous shorebirds and cassowaries and in buttonquail.

More likely to happen if the females are big, and therefore not likely to get beaten up by an outraged male; and dominant. And in humans polyandry is actually culturally driven, and it's associated with co-inheritance of farms by brothers; and that happens in Tibet and Nepal.

So here are four brothers who share one wife. And that is a very kind of agriculturally restricted mating system, and it has to do with inheritance rules. And you'll find in cultural anthropology, if you go around the world, that those kinds of culturally inherited inheritance patterns really have a fairly large effect on human mating patterns and parental care patterns around the world.

So dowry societies are quite different from bridal gift societies, and where all the brothers in a family can only inherit one farm, and space is restricted and life is harsh. Those things make big differences.

Chapter 4. Social and Reproductive Influences upon Parental Investment [00:26:55]

Okay, how do reproductive conflicts interact with parental care? Well we've already seen that there can be parent-offspring conflict over parental investment. So that can lead to issues of sex allocation in chimpanzees. You'll recall the Trivers-Willard hypothesis which said that if you are a dominant female, you want to invest more in sons, and if you are a low-ranking female, you want to invest more in daughters.

Because in a society that has a dominance hierarchy that gives high ranking males better probability of mating, and therefore better probability of grandchildren, you only really want to invest in males if they're going to have a good chance of rising in that rank, and that would be because you yourself, as a female, are already dominant; that gives you a good predictor that your son might have high rank as well.

Whereas if you are a low-ranking female, in poor physiological condition, then you don't really get very much out of investing in a son that will have little prospect for mating. But you can still get grandchildren out of investing in daughters. So we've been through that for chimpanzees.

We've also discussed how male-female conflict over parental investment will lead to pregnancy conflicts that are mediated by genomic imprinting in humans; those are David Haig's ideas, as further developed by Bernie Crespi. And there can be sib competition conflict over parental investment that will lead to analyses of brood reduction.

So it's a fairly common observation among raptors--eagles, and among herons and their allies, egrets and herons, and among owls--that they will lay a clutch that has significantly more eggs in it than they can possibly fledge. The babies will hatch. The parents are not able to feed all of them equally well. The babies will fight with each other for access to food, and they'll actually kill each other; so that out of one of these nests, where maybe four to six eggs might have been laid, you'll get one to two fledging offspring. And while the siblings fight with each other, the parents do not intervene; they just stand back and they let it happen.

So the kin selection argument on this is that offspring want more parental investment than the parents want to give them, because the parent has 50% relationship to all offspring. The offspring is 100% related to itself and 50% related to siblings. So on this assumption you should see overt conflicts between parents and offspring; and that's broadly confirmed. Okay?

Usually at weaning and fledging the offspring are complaining and the parents are shoving them away. And this kind of conflict is won by the mothers in chimpanzees. You should see offspring that are soliciting their parents and actually causing their parents to exceed their optimal level of investment and reduce parental fitness. This doesn't really seem to happen too much.

But in the social hymenoptera one can see that the colonies are producing sex ratios that are optimal for the offspring rather than for the parents. So there's a fairly complex theory of what the sex ratio should be of a social insect colony, based on the interests of the workers, versus the interests of the queen and the king. And there are skewed sex ratios that come out of colonies reflecting worker interest. So sometimes the offspring do seem to be able to take control of that aspect of parental investment.

There's another prediction, which is that the offspring should solicit to a level that would actually cause them to have significant costs. So you should see the offspring trying really hard, to the point where they're paying costs in terms of their own fitness in order to get more investment out of parents and essentially blackmail them into not investing in other offspring. There's very little data on that.

So Bob Trivers is the guy that when he was a graduate student at Harvard, and a junior fellow at Harvard, and was a young father with children, came up with the theory of parent-offspring conflict.

I mentioned that raptors are birds--this is a survivor of a parent-offspring- of an offspring-offspring conflict. But it is set up by the parents. Remember that if you have siblicide going on in nest of eagles or hawks or egrets or herons, that it is the parents who have decided that there will be a competition in that nest, and they have done it by laying that many eggs into it. So this is something that's going on in the lifecycle of just about every single one of these raptors. They have been through a very, very stringent period early in life. And of course in female hyenas there is something like that that goes on. So this is a case where we have all kinds of behavioral ecology and evolutionary ecology coming together.

So hyenas are a case of female reproductive dominance. In the first week of life, the sisters fight viciously with each other. I learned last night that this happens in the Iberian Lynx as well. One of the reasons that it's difficult for conversation biologists to save the Iberian Lynx is that there are only a hundred of them left. And they get a female into the breeding facility and she gives birth, and when the cubs are one-month-old, they start to kill each other. And that lasts for about a month; they just go at it, and usually there's only one survivor.

The same thing happens in hyenas. It appears that there's over-expression of testosterone. Well we know, we've measured it; not me, but Lawrence Frank and others have measured testosterone levels during pregnancy, and there's over-expression. And that leads to male mimicking genitalia. This is now used by females in dominance signaling, and it does have some consequences for copulation and birth in hyenas. And I think some of you have read one of the critical papers about this scenario. Okay?

So the female hyena's reproductive tract has been heavily modified. Here is the embryo here, and this is her clitoris, which has now been modified developmentally by the over-expression of testosterone when she was in utero, and it is used for dominance signaling and things like that.

This pattern--by the way, in a group of adult hyenas, there will be a dominant female, some subordinate females, and some males who have pretty subordinate behavior, and it's normally the dominant female who's doing most of the reproducing in that group. So there's reproductive suppression.

And we'll now look at a couple of other cases of reproductive suppression. One of them is in dwarf mongooses. And this is a pretty radical case of behavior. Okay? The dominant female does most of the breeding, and being in the group is quite critical. They have packs of about eight to twenty individuals. This is one from a big pack. Okay? They are voracious predators. They can eat lizards and snakes and spiders and scorpions.

And this is the remarkable thing about them. If a subordinate female dwarf mongoose has made a mistake and gotten pregnant, and gives birth, and she's confronted by the dominant female, she'll go get the offspring and take them to the dominant female, who kills them. She goes and gets her babies and delivers them to the dominant female. Okay?

So this to us is really a radical and upsetting thing; and it's just about the opposite of male suicide in red-back spiders. Because what's going on here is that subordinate female, in this reproductive system and under these ecological constraints, is only going to be able to reproduce successfully in a group; and in order to do so she's going to have to survive long enough to become a dominant female.

The only way she can survive is to stay in the group, and the only way that she can become dominant is to stay in the group a long time. If she goes around having babies, she's going to get kicked out of the group. She will die and her babies will die. So if the option is either both of us die, both me and my babies, or only my babies die and I survive to try again another day, then they make the best of a bad job by doing this. Okay? It certainly isn't optimal, from any interpretation, but it's probably the best that a subordinate female can do under the circumstances.

You wouldn't think that this kind of thing would be going on in the social life of something that looks so fuzzy and lovable; you know, they really are rather cute. But similar things are going on in meerkats, which are their relatives; you know, these highly social mongooses that Tim Clutton-Brock studies. And it's just amazing how much brutality and crime can be--you know, from the human point of view--can be packed into the head of something that's so fuzzy and lovable.

Chapter 5. Conclusion [00:37:05]

So let's go back to our original questions. What are the benefits and costs of parental care? Well the benefit, of course, is offspring survival, and the cost is parental survival. So we've seen with things like lump-suckers that the males will die protecting their babies.

So why does it vary so much among species? Well the payoff of having a few well-cared for offspring versus many poorly cared for offspring varies a lot, and it varies a lot both because of the incidence of predators and parasites and diseases in the different kinds of environments, and from the phylogenetic inheritance that's shaping the biology of those particular kinds of things.

It's not as though the environment in which these babies are living is given by Nature; it's something that's been constructed by evolution. So many things have co-evolved to create the situation in which this payoff is either large or small.

So why is it that the females do it in some cases and the males in others, and both? Well whether fertilization is external or internal is quite important; and that really does explain a tremendous amount of what we see in fish. But in things like birds and mammals, this is all tied up with social evolution and the evolution of breeding systems and with sexual selection and things like that. It's because in birds and mammals everybody has internal fertilization, and it's other things that are involved in explaining who takes care of the babies.

Why is it that parents will sometimes kill or neglect their offspring? Well, you know, the simple explanation is the standard adaptationist/evolutionary explanation: they do it to increase their lifetime reproductive success, and that means that there must be some very intriguing tradeoffs and some very strong social and ecological constraints; otherwise you wouldn't see them sacrificing direct fitness for long-term gain and fitness. But exactly how that works depends on the case under discussion. Okay?

Now humans do this, of course. Humans will have spontaneous abortions if the MHC genes of the mother and the father are very similar to each other. So in fact the human reproductive tract is set up to carry out this sort of thing, and the human cultural system will cause this to happen, with very high rates of female infanticide in cultures that have high dowries and other reasons for favoring boys over girls.

So the excess of boys in China is estimated at about 30%. So there are about 130 boys for each hundred girls, that are recorded in China; especially in rural China, not so much in the cities.

And that's what I mean by exactly how that works depends on the case under discussion. It can be the immune system; it can be the inheritance pattern; it can be the social system, with raptors and things like that. It can be driven by food supply and a lot of such things. Okay, so next time we'll talk about alternative breeding strategies, and if you're interested I can go to lunch today.

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