EEB 122: Principles of Evolution, Ecology and Behavior?

Lecture 34. Mating Systems and Parental Care

https://oyc.yale.edu/ecology-and-evolutionary-biology/eeb-122/lecture-34

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. 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.?

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. 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.?

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.?You can store food.?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.?They can eat secretions produced in special brood chambers, or they can get nourished via placentas or pseudo-placentas.?

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%. 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。

This is a frog, the Coqui frog from Puerto Rico and?it has male parental care, and 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.?

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.

It can be quite risky to guard a nest. 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?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, a female is?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.?

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, adelphophagy.?

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.?

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 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. It has a really very interesting life history. It just gives birth to one offspring at a time. Most flies will go around laying?fifteen, twenty, fifty eggs a day.?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,?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 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.?And, of course, seahorses have lots of other wonderful things.?

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.?

There is a relationship between the mating system and the pattern of parental care.?

• 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 polygynous 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. So sticklebacks, lump-suckers, gobies, things like that.

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?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?she doesn't really, she sticks around.?

• The swans, which are monogamous, and then the dunnocks, which are polygyandrous, are cases where both parents will care for the offspring.

• 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. Elephant seals also?have harem defense. But it's a special case with a broad-leaf foraging ungulate. 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.?

• 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.

• 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.

• 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.?So how could that happen? How could you possibly get into polyandry and then possibly from that go into monogamy?

• 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?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 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. It?is a very kind of agriculturally restricted mating system, and it has to do with inheritance rules. 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.?

How do reproductive conflicts interact with parental care??

• 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.

• We've discussed how male-female conflict over parental investment will lead to pregnancy conflicts that are mediated by genomic imprinting in humans.?And there can be sib competition conflict over parental investment that will lead to analyses of brood reduction.

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.?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.

• 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.

• 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.?

I mentioned that raptors are birds?of an offspring-offspring conflict, which is?set up by the parents. 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. 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.?

• Hyenas are a case of female reproductive dominance. In the first week of life, the sisters fight viciously with each other. 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.

• It appears that there's over-expression of testosterone. 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.

• 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.

• 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.?

• In dwarf mongooses,?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. They are voracious predators. They can eat lizards and snakes and spiders and scorpions.

• 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.

• 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.?It certainly isn't optimal, from any interpretation, but it's probably the best that a subordinate female can do under the circumstances.

So let's go back to our original questions. What are the benefits and costs of parental care? 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? 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.?

So why is it that the females do it in some cases and the males in others, and both? Whether fertilization is external or internal is quite important.

Why is it that parents will sometimes kill or neglect their offspring? The simple explanation is the standard adaptationist/evolutionary explanation: parents?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.?

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.?

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.?