#914 Eduardo Fernandez-Duque: Mating Systems, Biparental Care, and Cooperative Breeding in Primates

00:00 Ricardo Lopes: Hello everybody. Welcome to a new episode of the Decent. I'm your host as always Ricardo Lobs. And today I'm joined by Doctor Eduardo Fernandez Duque. He is Professor of Anthropology at the School of Arts and Sciences with a secondary appointment at the School of the Environment at Yale University. He is a biological anthropologist with the g real interest in understanding the evolution and maintenance of social systems. And today we're focusing mostly on mating systems in private, by parental care, co-operative breathing, natal dispersal and some other related topics. So, Doctor Fernandez Duque, welcome to the show. It's a big pleasure to everyone.

00:39 Eduardo Fernandez-Duque: Thank you Ricardo. It's a pleasure and the pleasure is mine. It's been an impressive program that you've been developing over the years. So I'm honored to be joining the, the host of speakers you've had in the past. Thank you. Well,

00:51 Ricardo Lopes: thank you so much for the kind words. And so to start off with uh what different kinds of mating systems do we find across primate species? Exactly.

01:04 Eduardo Fernandez-Duque: So, uh before I answer specifically that I'd like to make the distinction, it's gonna help us in our conversation later on between social systems and mating systems. OK. And this is one of those times when maybe relating it to humans really helps us get the message across. So we, we always try to be very careful when we move between monkeys and humans. But a social system, it's, it's the kind of situation in which individuals of the different sexes and different ages interact with each other socially, behaviorally, demographically, but without any explicit reference to where they are mating with each other, whether whether they are having sex with each other or not. So, when we talk about a mating system, we're referring to in a very general sense who has sex with whom. And again, further on, I suspect we will be elaborating a little bit more on the differences between having sex and actually reproducing with each other. But we can come back, we can come back to that later. So if we're gonna talk about who has sex with whom who, who met with whom in, in primates, uh you have them of all kinds. Uh Most people are very familiar with those species where you have several adult males and several adult females and they're all mating with all of, I mean, with each other, there are patterns, of course, sometimes a male will concentrate most of the mating opportunities and other males may not be so lucky. Uh BUT usually made most of the females do have access to mating. So we talk about those groups as being multi male, multi female mating systems. We may also refer to them as polygynous, meaning that one male has access to many females we have in primates as well. A system that's very rare uh in, in most animals definitely rare in primates and in humans, which is a system where a single female may mate with many males polyandry. And it's in primates, we only see it in some relatively small primates monkeys of South America. And then we have another system, which is the system where I have focused my research, which is a system where there is monogamous mating, meaning that there's only one adult male mating with one adult female. It is usually the case is that when that happens, those animals also have some kind of socially monogamous system. They are just spending time with each other. So that in a nutshell, it's a little bit range, big variation that we see in primates for mating systems.

03:52 Ricardo Lopes: And what do we know about the factors that influence mating systems in primates? That is if for example, in a particular species, we find that polygyny, polygyny is dominant or monogamy is dominant or any other kind of mating system, what are the factors that influence that? Exactly.

04:12 Eduardo Fernandez-Duque: So it would have been interesting to have my response to that question, say 57, 10 years ago, it would have probably been different from what I'm gonna say. Now, I am finding myself in the last many years, immersing more and more into what is known as the causal revolution, uh reading and teaching and writing about causal inference. I'm trying to really embrace the uncertainty that comes from the research we do in primatology. Most of our research is observational. Therefore, really talking about the factors that influence sometimes convey to the public an understanding that we have about the relationship between presumed causes and effects that we do not have. So having made that clarification that we, we be talking about factors that influence what we really mean. What we study primates, living primates in an ecological setting is what are some factors that we see happening in a certain relationship in a certain association with these mating systems that we observe having made that clarification, which sometimes of course, we're talking about mating systems in primates. Maybe it isn't that serious if we do not get the causal pathway correctly. But it is profoundly important, the the misunderstanding we have in making causal influence claims for very, very important social matters that we're interested in. So what are some of the factors the the the the typical culprits have been, of course, all kinds of social and environmental factors and a very, very general hypothesis that it is so general that you cannot really test it adequately is that when you have resources that are distributed in space in a re relatively homogeneous manner, there may be a situation that lends itself to a higher probability of having a monogamous mating system. Why? Because in mammals and this is very, very important in mammals. Let's not forget that male and females have very, very different reproductive biology. Females have a pregnancy and females lactate males do not. And so I think a very reasonable assumption is that that conditions so much of the social systems and mating systems of all mammals, primates included. So if the resources say food are evenly distributed in space, the assumption is that it is likely that females will distribute in space also evenly because they only need that similar amounts of food. And it is the distribution of females in space that may condition that may influence if if we allow ourselves to speak in that matter how males may seek females and how males may organize themselves spatially socially in terms of mating with females. So we look at the environment to understand pa patterns of mating systems. Then of course, you you always have these questions, the, the egg and the chicken uh challenge because what comes first is very, very different, difficult to disentangle in living systems. And so there's a lot of data suggesting that it is more likely to have a monogamy in those systems where you can also recruit, engage the contribution of the male to the care of the young. Because once you get that, we're gonna be talking about that assume later on by parental care or paternal care, then there are higher benefits to both the male and the female from sticking together than if the male were just to mate with one female now and with the second one later, so we look at social factors, we look at ecological factors, we look at environmental factors when I'm referring to factors that we can actually measure in real time in the field.

08:15 Ricardo Lopes: And uh when it comes to monogamy, specifically, there's this distinction between social and genetic monogamy. So what's the distinction? And why does it matter?

08:29 Eduardo Fernandez-Duque: The distinction is again, very, very simple to understand for us humans, there is a difference between with whom you have sex and with whom you have kids, raise them, protect them and contribute resources. So before the genetic revolution and by that, I mean, what started occurring now more than 30 years ago that we are able to obtain samples from the wild animals. We studied to do genetic analysis before that we had nothing but looking at who was mating with whom. So you would have found a group of all monkeys uh with a lot of dedication, maybe you were able to identify who is the male, who is the female that's very, very difficult to do in this tax because males and females look the same. And then you would conclude that male a only mates with female. A and so you would call that a social monogamy. You may also call it monogamous. Ma but the truth is that we didn't know where that mating really resulted in pregnancies and births. It was through studies of birds which are primarily monogamous. Most mammals are not monogamous. Then we started learning about what has become in the literature called EP CS extra pair populations. And then we added a fertilizations to that because an extra peer population was described, as I see this female who is socially paired to this male mating with the male outside the peer. That's an extra peer population. Before genetics, we couldn't still determine where that extra pair of copulation led to having an infant with genetics. We could and we started seeing that a huge, huge numbers of bird species that have been described as socially monogamous were not genetically monogamous. It wasn't true that a male and a female were only reproducing with each other. They were mating with each other, but they were mating also with other males and other females. There have been attempts, I mean, people have done the same kinds of studies with all kinds of primate species. And that's how we learned that even in those systems that I was describing before, where you have many males and many females mating with each other living with each other, many times you have sub reproductive skill. What we mean by that is that it is usually one male who actually sires most of the young even when the others may be getting a bite here and there, they are not really carrying the weight of producing the next generation of individuals. We have several talks among primates that are peer living where we see social monogamy and we have some primates where people have evaluated generic monogamy. Uh Our project is probably one of the largest, if not the largest attempt at characterizing social and generic monogamy in a nonhuman primate. And much to our surprise, we have found that consistently for all monkeys in Argentina, it is just that male and that female who are sharing a space, who are sharing a home, who are sharing feeding activities that are only producing infants with each other. We have never ever in all these years and now we have evaluated over 100 pairs of putative infants and fathers never have. We found evidence of extra pair population always the male to whom we are, which to whom we assign paternity. It has always been the male that was in the group with the female at the time of conception and pregnancy. I have studied with colleagues in in Ecuador and other socially monogamous primate, the TD and saki monkeys with, I mean, we studied this with my colleague, Tony Di Fiore with Saro Bell Marian Cook. We have looked at other primates and in those cases, the evidence is not as unequivocal that you have genetic monogamy. In fact, our monkeys are today one of the very few mammal species where you just don't find any extra pair paternity. It remains a puzzle. I am not convinced. I mean, if you ask me, I bet my money that sooner or later we're gonna find some data, some, some evidence suggesting that every so often there is some extra per attorney but so far none that we have found.

13:31 Ricardo Lopes: And so at a certain point there, you mentioned pair living. So could you tell us a little bit more about what pair living is? And is it related in any way to pair bonding or not

13:45 Eduardo Fernandez-Duque: peer living? And, and I, I think I didn't address before something that's going to be important for discussing peer living. Why it matters, the distinction between social and genetic monogamy, it matters because it helps you understand the pe living. So, I mean, e evolution depends on, on you passing traits that are inherited by the future generation, right? That's how traits become more abundant in the population, how they become fixed or not. So, really what matters if there's some biological basis to the tendency to live in pairs to focus your attention, your mating and reproduction repression with one single adult be male or female, it needs to pay off in terms of reproduction of fitness. That's where the genetic monogamy is important. What we mean by peer living is now going back to the social system is that consistently everywhere people have looked at all monkeys, everywhere people have looked at titty monkeys from Panama down to Argentina all the time. We just find one adult male and one adult female and they function very cohesively. They go about their lives very close to each other. Traveling. I mean, most of the times if you go to the forest in Ecuador, in Peru, in Argentina, you'll find TD monkey adults and old monkey adults within 3 5 m of each other max every so often they may be further away. So they're really close to each other. They are coordinating their activities. One is feeding more most likely the other one is feeding, one is sleeping, the other is sleeping and very importantly, they're also coordinating and sharing parental duties. They take care of the young together. You ask a question about how peer living and peer bonding relate. They relate a lot. But here is where I am guilty of sometimes having discussed peer bonding in all monkeys in the field without really having the robust evidence for a pair bond that we may have for some pair bonded mammals in captivity. This is a good opportunity for me to discuss how important how enriching it is to combine what you can learn from studying animals in the wild and you can what you can learn from studying animals in captivity. Our monkeys function in the wild in a way that it is suggestive of having a very strong pair bond. When we talk about a pair bond, we are usually implying some kind of physiological process by which two individuals, let's talk first about a bond. People are very familiar with the bond between a mother and an offspring. Not so much, not so much familiar, the bond exists between a father and an offspring. What do we mean by that? What do we mean by the mother offspring bond? We mean that there's some physiological process by which those two individuals are emotionally attached. There is some extent of dependency of one on the other and vice versa. There is usually some anxiety, some stress if that relationship is terminated, right? The same happens with an adult male and adult female in many bird species. And in some mammal species including the titty monkeys that my colleagues led by by former advisor Bill Mason Sally Mendoza. And in the last 20 years, caring males have studied in great detail at the California Primate Center in the US. So we have evidence for TV, monkeys that the male and the female are emotionally connected, they, they seek each other, they prefer each other and they are stressed when they cannot count on each other. Do we have those data? Do we have the kind of detailed data my colleagues have for TD monkeys which I studied back in the day for the gual monkeys? No, we don't, but we allow ourselves to make the inference that their behavioral patterns seem to reflect what is probably a physiologically driven, maintained pair bond. Uh THE, the, the, the very, very rich but anecdotal evidence we have of this in the field is that for 20 years, we have regularly captured one of the two adults in the pair to feed them with a radio color. And when that happens, when you take the male or the female from the pair, there is quite a fascinating response by the remaining adult who doesn't run away, stays near the place where we doing the physical exam of his or her partner calling. So that has been, we never planned this. It so happened, we need to do it. That has been our little semi experiment of disrupting the relationship and assessing how the partner left behind responded. So that's what I mean by peer living pair bonding. Uh We do see also behavioral evidence of what seems to be a very strong attachment of the infants to the fathers, something that we know as well from TD monkeys in the field and in captivity.

19:25 Ricardo Lopes: So I guess that perhaps this will be a good point to introduce the topic of bi parental care, which is something that we've already been alluding to several times in our conversation. So what conditions favor the evolution of bi parental care

19:43 Eduardo Fernandez-Duque: by buying parental care? Of course, we're referring to a system of care where both parents provide care very, very frequent, say in birds, very frequent in fish, but not so frequent in mammals. But remember birds and fish do not have a pregnancy, do not have lactation. So, uh mammals like in primates, like in our monkeys and tty monkeys, the expectation is that ok, maybe we do not need a male as long as the female carries on a successful pregnancy and then nurses the infant. That's all it takes because in fact, we do see that in a lot of other mammals where the involvement of the male is, is trivial or non existent. But that isn't the case in titty monkeys, our monkeys and also Khali Rich, which is another group of primates from South America. In this taxi, this range of species, the male is actively involved in providing care to the young. What is it that the male does when you were asking, let me describe what we mean by by panel care that we get into. What is it that may be favoring the evolution of this in the case of a Maki anis is quite remarkable when I'm asked, what is the single, if, if, if I had to choose one single characteristic of alma anti mais that makes them unique. I think it is without any doubts, the commitment of the males to the kid of the young. I know of no other mammal on earth where the males are as committed as fathers, as titty monkeys and owl monkeys. Just from a few days after birth, the male will actively seek to engage to interact with a newborn for the first time in 27 years. Now, 18 months ago, we saw a live birth in the forest of Argentina sometime around 11 in the morning. And for the first time from a wide group of all monkeys, some assistants were able to see how the male was right there. It was like having the male in the, in the same room in the delivery room. The baby is not yet completely out of the mom's wound and the father was there licking sniffing, interacting with mother and the infant a few days after the infant is born, the male may also get closer to the female and between them both, they may transfer the infant to the male. And I wanna say a week definitely two weeks after the infant is born, most of the times the infant will be transported, carried by the father. So here I'm using male and father for the Almay of Argentina quick and confidently call it the father. We know it is the genetic father and that relationship goes on and it goes on through, through the through infancy, through the juvenile period. Even through s adulthood, we have very robust data showing that there is from all these various stages of development. The young prefer to approach to interact to socialize with the father more than the mother. In fact, through research done by, by Doctor Alva Garcia de La Chica from Spain who who did her phd and a postdoc with the Almay Project. Her analysis has suggested that there are bigger consequences to the survival of the young when the father dies than when the mother dies. So that's where bipart care is. This very profound, a commitment of the male to providing care to the young, the male and the female coordinating you. You need to be close to each other, right? Because it is still the female who carries on the the burden of lactating. And we know that's energetically costly. So male and female really have to be peer living and coordinate their activities. If, if mom were nursing the infant and when she's tired of it, the male were ranging a mile away, seeking another female, it wouldn't work. You really need to have a two, a two person system at home. And so we think that I go back to what I was saying before about the chicken and the egg is very, very different to disentangle what favors what. But when you look another way in which we can make inferences is to look at the distribution of these phenotypes of these traits across the animal kingdom. And consistently, we see that it is much more likely that you get by parental care when there is peer living and peer bonding than the other way around. So evolution is speaking phylogenetic speaking, there seems to be reasons to suggest propose that you need to have coordinating peer living, peer bonding. Why? Because that means proximity. That means emotional connection. That maybe means faithfulness. Once you have those conditions settled, then it is much more likely that the male may be favored if you were to invest energy on the young. Because by being close to each other, you reduce the chances of the extra pair populations. We were discussing before. If I have been with my partner all along, then the chances are much higher that I have actually sired that young. So, evolutionary speaking, it pays off that I invest energy in a young that I have sired as opposed to maybe a mating system. Like we were describing at the beginning where you have males and females mating with several members of the other sex. So for mammals that we looked at when we examined some data in the literature, this was a study led by my colleague, Marian Hook where she reviewed the evidence we had for social monogamy pair bonding and parental care in mammals. It is usually when you have closely close pairs as opposed to these first pairs that it is more likely you get by parental care,

26:14 Ricardo Lopes: right? And so when it comes to things that we've been talking about, like for example, per leaving sexual monogamy and bi parental care, do we know if a sexual selection plays a role in their evolution?

26:35 Eduardo Fernandez-Duque: Yes. So, so keep it I choose between. Yes and no. Let's go with. Yes. We have decades and decades of research. On sexual selection, uh and with a range of taxa, and sometimes we know, or we allow ourselves to feel that we have a very solid understanding because it has been shown in other taxa in other systems where it is much more likely to really make the manipulations that allow you to get closer at understanding the connection between sexually selected traits and a particular mating system. Uh One of the areas where people have looked, a lot of potential relationships between factors is body size dimorphism. Uh We, we as we have a lot of data indicating that certain traits in ma and femurs are sexually selected. It's very interesting that in pure living primates, we do not have a lot of sexual dimorphism. And so an argument has been made and I think again, there's a lot of data across tax uh suggesting that maybe sexual dimorphism is related to sexual selection. We do not. Uh I was saying before how difficult it is, we cannot really tell males from females without monkeys and TV monkeys. And this is just to give you an indication of how complicated it is at the California prime etcetera where I did my phd studying T monkeys even today in captivity where you're looking at the animals say from, from 2 m away, they tag the males and females with different tags. It's an exon tag for the males, I think and a circular one for the females because you can be standing in front of them and you cannot tell them apart. So we cannot do that either with the al monies in the field. Uh Now going into the genetics of sexual selection, that is much more challenging. And that's where there's still so much that we need to do identifying traits for which we know the genetic basis that are related. For example, to the tendencies to provide care in males and females. We we don't really have that information in Almay or for any primate, the way in which we approach that is to look maybe at endocrinological profiles associated with parenting in the K rids that I was mentioning before that also have peer bonding and they also have paternal care. My colleagues, I'm thinking of Tony Ziegler or Jack Snow on. But I'm being unfair to so many of my colleagues who can work with the electrics in captivity. They have shown that in these males that provide a lot of parental care, sometimes you have some of the same hormones and same hormonal levels that you see in mothers who are providing care. So it is a very reasonable assumption that there has to be some genetics underlying these hormonal profiles in males and females that are so similar in situations where the male and the female are both providing care. But but it's still, I mean, behavioral genetics as we call it, understand the true genetic basis of complex behaviors like infant care or peer bonding. Uh We are still very far from understanding how those things, how those trades get selected.

30:07 Ricardo Lopes: So I would like to ask you now a little bit about co-operative breathing. Uh ON the show, I've already talked with several anthropologists over the years uh about the cooper breathing in humans in human societies. I don't know if you also want to get a, a little bit into that. But does it also occur in other primate species?

30:30 Eduardo Fernandez-Duque: Yes, it does occur. Uh Let's, we, we can look back to the first question we were discussing, which was the range of mating systems we have in primates. And I, I remember, I, I told you how, well f first, very basically, what do we mean by competitive breeding? And, and of course, among us, biological anthropologist and, and we can qui like about that, we end up writing reviews about, but for the purpose of having a fun conversation, let's decide that the definition is rather straightforward. To me. Cooper breath, you have a number of individuals cooperating in the taking care, raising of the young in a given group. Uh In some situations, people would argue that you have cooper breeding where there's only one female who's the one reproducing and then males in that group, but also relatives, siblings and grandparents and grandmothers and grandfathers are all helping. We do see not it down monkeys and the titty monkeys. Let's address them first because they leave us with a very interesting topic that we have not fully explored. Siblings don't help in our monkeys and titty monkeys. So you have your peer living species. Mom, dad, a couple of, there's an infant, there's a toddler and I have some juveniles and some adults and we just have no idea why their help is not recruited. It doesn't happen in captivity. It doesn't happen in the wild. It doesn't have importunities for all monkeys. But in other taxa in the calitri of South America where mom may have twins with some frequency and sometimes they may have twins a couple of times a year. The siblings help and more than one male may help take care of those young. So yes, we do have the kind of situation that has been used to refer to cooper breeding in humans. It takes a village, well, maybe not a village for the colored treats, but definitely more than mom and dad, mom, dad, siblings and some other females and males who may be related to those young. But for us, it's something we, we need, we need still to explore. Why don't the siblings in our monkeys and TV monkeys contribute. Uh Yeah, it's interesting. I imagine they're probably better off just putting all that energy into growing healthy and preparing themselves for competing in securing their own mates in the future.

33:14 Ricardo Lopes: By the way, when it comes to co-operative breeding, and now we're talking mostly about other primate species and not so much humans. Do we know if there is always necessarily some sort of genetic relatedness between uh the cooper breathers and the infants or not?

33:37 Eduardo Fernandez-Duque: We don't have a lot of data for that in the Colored Treaties, but there are some studies uh reporting that there is relatedness. Uh I have to admit the, the names of my colleagues who led those studies are escaping me. So we have some data for the colored trid in terms of relatedness now with non humans. What's also what's interesting I think is that if people have asked me if we were to swap, I mean, if you were able to take an infant out monkey and remove it and bring a substitute, would it change? My guess is if you did it right away from the go I, I'd be surprised if the father, if the male doesn't take care of that young, who is not now, not his desire. Uh So uh yes, we do have information on relatedness and it because we know that sometimes it is, for example, in the colored rich, sometimes it is brothers who help take care of the twins that the female has sired. And sometimes we have in colored rich. Its that more than one male is really mating with a female. That's why I was saying before that in those systems, we have what we call polyandry. The female mating with several males. So that would be a potential explanation for why those males may be helping because again, there is a likelihood that they have sired those young.

35:06 Ricardo Lopes: Mhm. And do we know exactly what predicts the evolution of co-operative breeding in particular species?

35:16 Eduardo Fernandez-Duque: No, we don't know anything very precisely. That would be. No. But really, I mean, that, that's the another conversation we can have one day we need to tone down. And so we go into the classroom and teach our entry level students how science work and how science is self correct itself and we get it wrong and we try again, but we seem to forget about those lectures when we write the papers. So uh no, I don't know. I would again choosing between. Yes and no, I would say no, we don't. But so, so your question was, do we know effectively if cooper breeding repeat me basically

36:00 Ricardo Lopes: what factors predict the evolution of cooper breeding in particular species?

36:07 Eduardo Fernandez-Duque: Uh No, I think we, it's, it's I I'll try to answer it the same way that we explore what we know about the factors that may influence the evolution of, of peer bonding or monogamy. Uh And so in humans, it's been argued that because humans as a species have so many life history traits that are so profoundly different from life history traits in other species, it may have been that by having cooperated breeding, that has completely redesigned the energetic balance of all the actors involved and may have allowed humans to have a rate of reproduction that's unparalleled with other taxa. Uh People have argued that maybe that's the reason that you also have in the ked riches which have cooperated breeding the production of twins. But the production of twins is such a rare event, at least for all the primates in the Americas that it is my understanding that that is still an unresolved issue. So people have argued have hypothesized that it probably is related to changes and the pros and cons and the tradeoffs in life history, traits of humans or other species with competitive breeding in relationship to those where there is no competitive breeding. But there have also been, again, it's making me think about your initial question on factors promoting monogamy for birds. People have examined the extent to which it is environmental unpredictability that may be related to the the evolution of competitive breeding in birds. Uh So uh many, many possibilities, many hypothesis. It is possible that for us to get closer to a more a better predictive answer would have to narrow down the scope of tax for which we're developing our hypothetical models. And instead of trying to understand the evolution of competitivity in birds, it'd be interesting to see what we learn, trying to go going narrower and deeper. I it's something that some colleagues are doing, of course.

38:17 Ricardo Lopes: So I have one more question about co-operative breathing here before we change topics. So is there any evidence that cooper breeding might favor in any way the evolution of enhanced social cognition or larger breeds.

38:36 Eduardo Fernandez-Duque: It has been suggested and, and there have been hypothesis proposed on that. Uh What is interesting? I am a little bit on, on the side of this intellectual, very interesting conversation. I have not really contributed any, any primary research to the to the debate. Uh My my impression is that the, it is not very clear. And if things get much more complicated when you go outside primates and look at other tasks to understand if it is really that competitive breeding uh is related to the kind of development of cognition and brain size that people have argued for primates comes to my mind. Uh STUDIES by Alex Thornton and and Kathy mccloud who have argued that they have all kinds of evidence from if I remember away from captivity on, on birds where maybe there is not as much data suggesting this. But I think again, it will probably make more progress in going smaller than bigger. Uh You cannot expect to have one explanation, explain the whole diversity of these patterns. But I'm not, I'm probably not as qualified to comment much on, on, on social cognition and larger brains. It's, it's quite outside my area of, of interest and ex of expertise. Definitely. Mhm

39:59 Ricardo Lopes: So let's get into the last topic of our conversation today. And I would like to ask you now about natal dispersal. What is that exactly?

40:10 Eduardo Fernandez-Duque: Natal dispersal refers to the process by which an individual leaves the area where it was born leaves disperses from the area where it was born. The natal area. And it is a very important process in the life of an individual because it's gonna have all kinds of consequences regarding its future. Social and mating interactions. Take, take it to an extreme if you're born in a family and you don't disperse. If you say I'm gonna stay poor, well, your opportunities for reproduction are gonna be limited most likely to your father, your mother and your siblings, and evolutionary speaking, we don't have reasons to believe that would be an evolutionary stable strategy. So animals disperse and when they disperse, which of the two sexes disperses or if both sexes disperses, it has been a very important area of research in behavioral ecology for all taxa in monogamous, impair living taxa, monkeys, primates, mammals, pers, you name them. The expectation is that both sexes ought to disperse. And that was the way it's been always considered in the literature because drawing from the bird literature for a long time, the assumption was that these pairs were living together for very prolonged periods, right? They were pairing for life. And so if the assumption is that the same male and the same femur are caring for life in this area, any offspring born to them or to the birds. So, so, so that they avoid mating with your parents as we learned in birds and in other tracks including primates, that pairs are not always long lasting. It is possible that now males and females may not disperse because their parents have been replaced. We have looked at natal dispersal in great detail. In good part letter by, by my colleague, Dr Maggie Corley who did her phd and then continued doing all kinds of endocrinological behavioral and genetic analysis on natal dispersal. And in the case of all monkeys like TD, we know that both sexes disperse, it kind of makes sense. But what we're learning now, what we're trying to understand is what are the possible reasons? What are the possible factors influencing when to disperse? And this is just work that we are, we're getting ready to publish, finally being able to look at the genetics and what Maggie we call Maggie Corley found is that there seems to be a tendency for the animals to disperse sooner or later in relationship to who of the parents are still in the group. Something we didn't talk about when discussing our monkeys and social systems is that the Almay population in Formosa allowed us to discover something that has not been reported consistently in, in many mammals, which is the existence of floaters. The animals who disperse don't get to find a partner right away, but the range alone is like mom, dad, I'm leaving. Ok. Go. What are you gonna do. I don't know, I'm gonna move around and see if I find a partner. And so they move around and they try to find a partner. But the problem is that we do not have in the Almay population in Formosa, anything like bars or these young adults moving around trying to find partners can get together and form a new family. So the solution the young monkeys are playing out is that my way to find a family is to really kick out from a home, the same sex adult who is holding control of their home. So a young adult male will challenge, fight and sometimes kick out a stable reproducing adult male and a young female will fight challenge and sometimes kick out a reproducing female. So now if you are the young who is pondering, do I disperse or not? You may find yourself that your biological father is no more. Now you have a stepfather or maybe you have a stepmother or maybe you have both stepfather and stepmother. And so that changes completely, completely. So many aspects of how we're examining behavioral patterns, demographic consequences of all these processes. Because what we're learning is that when for an owl monkey, when the parent of the same sex has been, I'm sorry, when the parent of the opposite sex has been replaced, they tend to stay longer. I'm a female and I'm pondering. Should I leave home or not? I suddenly I realized that that is not here anymore. Now, there is a stepfather, a stepfather that presumably are not related to. So that's the father may become every productive opportunity I stay longer. So those are analysis that we, we haven't published yet. We're working on it. But they connect the process of this pars the timing on this par with the genetics of group composition and in breeding avoidance.

45:46 Ricardo Lopes: OK. So let me ask you perhaps one final question. Then I think that when talking about owl monkeys and the timing of their natal dispersal, you focus there mostly on social factors, right? Are there any other kinds of factors like for example, ecological factors that might also play a role in explaining the timing of their dispersal?

46:10 Eduardo Fernandez-Duque: Absolutely. And we, we did look into ecological factors and environmental factors in our forest. It's probably not the ideal situation to examine those because we work in a very, very seasonal environment. So sometimes uh uh when, when things are so seasonal, there are some aspects of the life history of the animal that match. So you take, take the spring period. So the spring period is the period when the babies are born, but it's also the pure when food is more abundant. So, so it becomes complicated to these entangled factors. But what we're finding is that the environment is not as a strong predictor of when the animals disperse as maybe some social factors and all the social factors that we have been considering it is really relatedness which seems to be the the more predictive factor than others. But even when we see this parcel all around the year in Argentina, this parcel goes down, the rate of this parcel is lower in the winter when temperatures are lower and there's less abundance of food because one of the factors that seems reasonable animals in an evolutionary framework may have played a role is that you need to disperse at a time when you can cope with the disadvantages, not being in a social group. And one of the advantages of being in a social group can be things like thermal regulation. The the chaco region of Argentina gets cold and in the winter, you will see the animals huddling and sleeping together. Now, if you're on your own, wandering around at night, during the day, in a cold forest, maybe that may be a disadvantage that doesn't play to you in evolutionary terms. And the animals may be dispersing at a time when it's less challenging in terms of thermal regulation or in terms of finding enough food outside of your home.

48:11 Ricardo Lopes: Mhm Great. So Doctor Fernandez Duque, just before we go, would you like to tell people where they can find you and your work on the internet?

48:22 Eduardo Fernandez-Duque: Yes. Uh We have a, we have a website for the Almony project and if you just type that you'll come across that and I do have my own personal website that also provides links to the project to Fundacion Eco. Uh When I started my work in the province of Formosa Argentina, we established Fundacion Eco, which is an NGO that promotes education in the country. So you can also look there and, but I think either my site or the Almay projects, I should give you plenty of information for the Almay research. I'm very proud to say that as of this month. In fact, we have just published, I have just published an edited volume that summarizes 30 years of research on all monkeys from Panama to Argentina. This is a book published by Springer and it's available. The E book is free of charge and you can find all types of research data. 60 colleagues of mine, we have all put together uh spanning the research on our monkeys that has been done from Panama down to Argentina, including also research led by my colleagues in the US who have been working with our monkeys for a very, very long time. So Al Monkey book by Springer is a wonderful resource and it's available free of charge as an E book. You can find all you need about al monkeys there.

49:45 Ricardo Lopes: Great. So I'm leaving some links to that in the description box of this interview. And Doctor Fernandez Duque, thank you so much again for taking the time to come on the show. It's been a pleasure to talk to you.

49:57 Eduardo Fernandez-Duque: Thank you Ricardo. Pleasure joining you and thanks for the time and the opportunity to share all this information about our research.

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