Tag Archives: Behavioral ecology

Parents and personality in the animal world.

Animal personality is a huge topic in behavioural ecology right now, and it seems like you can’t shake a stick in the literature without hitting another paper on the subject.  You may have heard of the term before, but if you’re asking “what is animal personality?”, I’m planning to write on the topic more extensively soon and so I ask that you bear with me and keep an eye out for that.  For now, we can go with a sensible version that defines animal personality as “consistent individual differences in behaviour, in time and/or across contexts, for both human and non-human animals” (Dall, Houston, & McNamara 2004).  In non-scientist speak, this means (broadly) that animals show personality traits in the same way we think of when we talk about humans;  when we say “he’s an aggressive person”, we mean that no matter what context you find him in, the person we are talking about expresses aggression. In a boxing ring, aggression is appropriate, but while it may not be so appropriate in the middle of a grocery store he expresses it anyways.   The study of personality traits in animals, where animals who are aggressive or exploratory or shy in one context tend to be so in others, has exploded in recent years and the signal can sometimes get lost in the noise.  To that end, I want to highlight a new paper in the Advance Access section of the journal Behavioral Ecology by Adam Reddon, entitled “Parental effects on animal personality”.

Rat image by ressaure; used under a CC license.

(Full disclosure:  Adam is a friend from my Master’s lab, and he’s scary smart.  He’s currently doing his Ph.D. at McMaster with Sigal Balshine and publishing papers at a rate that most people can only envy.  If you’re looking for young behavioural ecologists – or scientists in general – to watch, he should most certainly be on your list).

The point of this paper, an invited forum contribution, is to link the large literature on parental effects and animal personality.  Parental effects (though most work has been on maternal effects) cover “the ways parents can shape their offspring’s phenotypes over and above genetic inheritance”, as Adam puts it.  These effects can occur in many different ways, which Adam does a nice job of reviewing;  examples include nest site selection, the amount of food provided,  hormone transfer by birds into their eggs (which can, among other things, manipulate how fast the offspring grows), social interactions, and providing opportunities for social learning.  One great example that he provides is of Norway rats.  Rat mothers will lick and groom their pups after they are born, and the amount of licking and grooming that the pups experience in the first week will have big effects on how well the pups respond to stress both physiologically and behaviourally.  Pups who were interacted with less tend to be “shyer, less exploratory, less social, less aggressive, and less dominant” throughout their lifespan (p.2). This is clearly a parental effect, because pups who were cross-fostered (adopted) to other mothers had stress reactions that came from the licking and grooming of their adoptive mother and did not correlate with their genetic mother. Paternal effects are also quite widespread, having been seen across taxa, including mammals, birds, lizards, and even waterfleas (Daphnia cucullata) and radishes.

Adam’s contribution here is to draw a straight line between the two literatures by connecting developmental processes to animal personality, treating personality as an outcome instead of the starting point.  As he states (p. 2-3):  “… the parents of a developing organism are in a unique position to guide its development and alter the offspring’s personality to better match the environment it will face”.   Parents have acquired information about the environment that may be useful to the child, and if they can translate that into paternal effects that change the offspring’s personality in a way that takes advantage of that information, they may enhance the offspring’s fitness (and by extension, their own chance of seeing grand-offspring).  A speculative example might go something like this:  parents experience a poor environment because they can’t find food, and this lack of food leads them to manipulate their offspring into having a more exploratory personality so that the offspring will have a greater chance of escaping the poor conditions of the immediate area to find food.  This would be a risky strategy, but the idea of being risk-prone in poor environments has a long history in behavioural ecology (especially in foraging, e.g. Stephens 1981).

The upside of this paper is that the connection between them is obvious and powerful, at least in hindsight .  As Thomas Huxley was said to have exclaimed upon learning of Darwin’s idea of natural selection, “how extremely stupid not to have thought of that”.  The link to paternal effects gives researchers working on personality one potential explanation for the variation they see and a paradigm to test experimentally, and will hopefully energize both literatures.  I was also under the impression from my readings that fitness differences in offspring phenotypes arising from paternal effects weren’t well explored (I’m open to correction on this!), so perhaps linking maternal effects to personality variation will provide more data on how these effects affect selection over generations. The only potential downside I can see is that personality research, so far, has been characterised by some confusion over terminology and methodology (which I will touch on in a later post);  it might take researchers in this area some time to sort out the best way to combine the two approaches fruitfully.  On the other hand, the most exciting moments in science generally emerge out of areas of confusion and doubt, so I hold out hope that exploring the effects of parental decisions on offspring personality will lead to great advances in our understanding of animal behaviour.

References:

Adam Reddon. Parental effects on animal personality (in press).  Behavioral Ecology.

Sasha R. X. Dall, Alasdair I. Houston, and John M. McNamara. The behavioural ecology of personality: consistent individual differences from an adaptive perspective. Ecology Letters, 7:734–739, 2004.

Anurag A. Agrawal, Christian Laforsch, and Ralph Tollrian. Transgenerational induction of defences in animals and plants. Nature, 401:60-63, 1999.

David W. Stephens. The logic of risk sensitive foraging preferences. Animal Behaviour, 29 (2):628–629, 1981.

Tagged , ,

What is an animal’s “choice”?

Image by loryresearchgroup

In behavioural ecology, we face a number of limitations in trying to ferret out the relationship between behaviour and evolutionary forces.  These range from the philosophical and theoretical (e.g. what makes a behaviour adaptive or an adaptation?) to the mundane and methodological (is that experimental set up really measuring aggressive behaviour?), and solving these problems is one of the most pressing tasks facing a behavioural ecologist attempting to make useful statements about a behaviour’s evolution.  However, while some of these issues are recurrent and obvious, others are more subtle and can sometimes slip under the radar.  One such problem is the topic of a recent paper by Véronique Martel and Guy Bovin, published recently in the Journal of Insect Behaviour and entitled “Do choice tests really test choice?”  (DOI: 10.1007/s10905-011-9257-9).

The thrust of their argument is that there is a difference between “apparent choice”, and “true choice”, which is driven largely by the fact that we can’t ask animals what they would have done under different circumstances.  As Martel and Bovin point out, animals may make one choice when presented with a particular set of stimuli, or resources as they call it (which may mimic natural conditions!), but express a different preference when presented with a larger set of resources, or when the conditions of the choice are changed.  They distinguish three characteristics of a true choice, only one of which is met by an apparent choice:

  1. The choice must be non-random, i.e. that individuals must choose one resource more often than the others;  testing only this criteria means that researchers are measuring apparent choice, while this is a necessary but not sufficient criteria for true choice.  (I would add to this that the choice probability should be fairly stable if the animal is made to choose under exactly the same conditions).
  2. The choice should be the same even in the “absence of a differential response by the resource” (p. 332). The authors state this to avoid situations in which the resource (e.g. a potential mate) is manipulating the choice of the focal animal, a problem which reminds me very much of the literature on animal signalling.
  3. It should be demonstrated that every resource is perceived, to avoid issues of sensory bias and the like.  It strikes me that this criterion will be hard to meet;  for example, if while testing mate choice the researcher tries to demonstrate a lack of bias by showing responses by the focal individual to each of the potential mates in isolation, how does that prove that one or more of the potential mates aren’t being ignored when the focal individual is given the choice between all of them?
As the authors state, meeting criterion 1 is sufficient for an apparent choice, but 2 and 3 are required for a true choice.  They spend the bulk of the rest of the paper giving examples of both apparent and true choice and elaborating the differences between the two.  It should be noted that they are not claiming that one type of methodology is “better” than the other;  in fact, they take pains to point out the pros and cons of both.  Here’s an example:

The importance of distinguishing between apparent and true choices depends on the objective of a study. If the objective is to establish which resources will be exploited under natural conditions, then the apparent choice is appropriate. If the experimenter wants to know which female will be mated by a male in a natural situation, then the results of this test (the apparent choice) will provide the answer. However, if the objective of the experiment is to establish the mechanisms of this choice, then it becomes important to look more closely at the results. If a male does not perceive a mated female as a resource because she does not produce sex pheromone, the male is thus inseminating virgin females as they are the only resource perceived. In this case, an apparent choice (the virgin female) is expressed, but this choice is the result of the non-perception of the mated female, which prevents this apparent choice from being a true choice. Measuring an apparent rather than a true choice does not remove the relevance of the test, but only modifies its interpretation. Consequently, it is important for the experimenter to state a clear question before identifying the adequate experimental setup to use.

I think that it’s important to mention here that the ideas expressed in this paper aren’t terribly groundbreaking;  a number of people ranging from economics to psychology to behavioural ecology have, at one time or another, made largely the same argument or a variation thereof (one example of a related problem is raised by a really smart guy, Jeffrey Stevens, in this book chapter here).  In fact, I’m a co-author on a paper currently in press at Behavioural Ecology talking about this issue from the opposite direction, wherein we argue that the mechanisms that underlie behaviour may be constrained and that these constraints need to be taken into account when assessing the evolution of behavioural outcomes[1].  I even made an argument very much like the one in this paper during my Ph.D. synthesis exam!

Having said that, I like the paper for its laser-like focus on raising awareness about a very specific part of animal behaviour and cognition that can seriously undercut the conclusions drawn from experimental or field work if the appropriate test isn’t matched to the hypothesis the researcher wishes to explore.  I suspect that their definition of apparent and true choices is incomplete and leaves out issues that will be hashed out in future papers, but if the journey of a thousand steps has to start somewhere, it’s not a terrible first stride.
——–
[1]. I’ll write more about this here when the paper is published.

Tagged , ,

Death in the nest: trade-offs rule the day.

Underlying many research programs in biology is the meta question: why is there more than one type of X?  (In continuous form, why is there variation in X?)  This question recurs in many areas of animal behaviour, and indeed in the entirety of the study of evolution itself.  Some examples include:

  • Why do animals show variation in “personality” – why are some consistently more aggressive, more exploratory, bolder, etc.
  • Why are there more than one type of male that females select between?  Why are some “attractive” and others “unattractive” – why aren’t they all attractive? (Sexual selection).
  • If aggressive signals like roaring can make other animals give up a resource or back down from a fight, why don’t all animals use the aggressive signal?  Why is there variation in signal type when all animals should use the same signal, which would then lose all meaning and be ignored?
  • Why do some animals invest heavily in each offspring while others produce as many as they can and invest very little in each?
The general response to most of these questions hinges on the idea of a trade-off.  In its most basic form, a trade-off involves giving up one thing to get (or avoid) another.  In particular, animal behaviour often hinges on cost-benefit tradeoffs.  It is desirable to have some trait or perform some behaviour, but doing so may come with a cost if we have too much of the trait or perform the behaviour too often or at all.   Examples of this litter the pages of any textbook in the biological sciences, from molecular biology up to zoology and ecology;  in particular, we can begin to address the questions I listed above by appealing to trade-offs:
  • Some personality types, like aggressive or exploratory, can confer benefits – such as always winning fights or being the first to find food – but also come with costs – such as the injuries from always fighting or the cost of being eaten while you try to be the first to eat.  Some individuals will be willing to make this trade-off, others will not.
  • The answer to this question has filled entire bookshelves, but here’s one tiny example:  in 1975, Amotz Zahavi published a landmark paper proposing that attractive males are “handicapped”;  they willingly trade off the cost of the handicap for the increased number of matings of come with it.  Zahavi’s “handicap principle”  suggested that this was a reliable indicator of quality to females because only some males would have the required quality (be strong enough, fast enough, etc) to bear the cost of the handicap in order to reap the benefit.
  • One of the most well-known answers to this question began the field known as evolutionary game theory;  at the end of the 1970s, the tragic figure of George Price and the eminent John Maynard Smith answered the question by showing mathematically how frequency-dependence could lead to a trade-off between Hawks, who are aggressive, and Doves, who back down at the first sign of trouble;  when Hawks are extremely common, their aggression leads them into costly fights against each other, which reduces the benefit of aggressiveness and makes Dove-ish behaviour more attractive.  But when Doves are common, Hawks get immense benefit with no cost by bullying Doves around.  (There’s actually significant overlap between this point and the previous, but that’s a topic for another blog post!)
  • An entire branch of evolutionary biology, life history theory, deals with questions like this:  in the face of limited resources, how do individuals make choices about the timing and sequence of events in their life to maximize their fitness?

This general pattern underlies the story behind a neat new advance-access paper from the groups of Alex Kacelnik and Juan Reboreda that manages to give away the good stuff in the title:

Ros Gloag, Diego T. Tuero, Vanina D. Fiorini, Juan C. Reboreda, and Alex Kacelnik. The economics of nestmate killing in avian brood parasites: a provisions trade-off. Behavioral Ecology, 2011.

Here, the question of types and the answer of trade-offs arises in the context of brood parasitism.  Brood parasites are organisms – birds, fish, insects – that relieve themselves of the responsibility of parenthood by tricking other organisms into doing it for them.  In birds, this usually takes the form of brood parasites laying their eggs in other species’ nests, where the enterprising young tykes then pretend to be the offspring of the unlucky suckers who are to play host.  Brood parasites can be specialists that only parasitize the nests of a target host species (or small group of species); an example of this is village indigobirds, who generally parasitise fire-finches (and who also display an interesting mechanism where the young copy the songs of the host species).  Generalists, on the other hand, will parasitise a range of host species;  cowbirds, for instance, are generalists.  Brood parasites can also vary in whether they eliminate the other offspring of the host that they have colonized (nestmate killing) or whether they attempt to blend into the crowd (nestmate tolerant).  To make this more concrete, take a look at this short video showing a newly-hatched cuckoo ejecting a reed warbler chick from the host nest:

The paper I’m talking about here explores an interesting question about brood parasites, namely:  why are some brood parasites nestmate tolerant while others are nestmate killers? Gloag et al. propose a mathematical model that explains this in terms of a “provision trade-off”.  Host nestlings can help the newborn parasite by stimulating the host parents to bring more food than the parasite could solicit alone, and if the parasite can outcompete its nestmates for that additional food, then it does better to let them live.  Thus the trade-off:  when the host offspring increase the fitness of the parasite, it lets them stay, but otherwise it kills its flatmates.  Gloag et al. take the time to break this trade-off down into its constituent parts, namely (in their words, p. 2):

  • The total provisioning rate stimulated by the whole brood, and
  • The share of the provisions received by a parasite nestling.
The simple model they derive shows that when the ability of a parasite to stimulate food provisioning by the host parents is greater than its ability to compete for food with its nestmates, the parasite will do best if it is reared alone and the murder spree begins.  This relationship depends on the interaction between these two variables;  in other words, “[i]f each host nestling causes a greater increase in provisioning than the amount it consumes, then the presence of host chicks would result in higher consumption for the parasite, even if a host chick takes a bigger fraction of the extra food than the parasite.”  The model helps to predict where each scenario – nestmate killing or tolerance – is plausible as a function of this intuitive trade-off.
VIRA-BOSTA (Molothrus bonariensis)

VIRA-BOSTA (Molothrus bonariensis) by Dario Sanches, on Flickr

Gloag et al. then use this model to explain differences not only intra-specific differences between specialist species in their level of nestmate tolerance, but also inter-specific differences within generalist species as well.  This would have been a good paper even if they had stopped there, but they then go on to test their ideas in the field using a generalist parasite, the shiny cowbird (Molothrus bonariensis). Working in South America, they searched for the nests of two types of shiny cowbird hosts, chalk-browed mockingbirds and house wrens, and set up two experimental conditions.   In the “mixed group”, the a single cowbird egg was placed among host eggs, and in the “alone” group, the cowbird eggs were placed in the host nest with dummy eggs so that the cowbird young would be reared alone.  They measured the food amount and quality brought to the nest from video recordings, and measured the physical quality of the resulting offspring (weight and tarsus length).  They also compared the mortality rates of the cowbird chicks to see if there was a difference between the conditions.  Their findings?

In our field study, nestmate tolerant shiny cowbirds encountered both sides of a provisions trade-off depending on the host used. When reared by chalk-browed mockingbirds, nestling cowbirds had higher food consumption, mass gain, and survival when alone in the nest than when sharing with 2 mockingbird young. In contrast, cowbirds reared in the nests of house wrens had higher food intake and growth when reared alongside 3 or 4 host young than when reared alone. (p. 7).

The results of their work suggest strongly that there is a trade-off at work here, and that the virulence of parasite offspring will be affected by the provisioning characteristics of the host environment.  Of course, they are quick to suggest that there are other factors potentially at work in differential growth rates, such as thermoregulation (larger broods can help each other thermoregulate) or size of the nestlings.  Nestling size is an interesting issue, because as the authors mention, cowbird young are larger than house wren nestmates but equal in size to or smaller than their mockingbird counterparts.  This may the competitive ability of the young either through physical competition between nestlings where size would be important, or because parents preferentially feed larger offspring.  (As a by-product, this also raises the longer-standing question of why host parents don’t do a better job at discriminating among their young for parasites in the first place;  for an explanation in terms of yet another trade-off, I’d refer you to this letter to Nature by Arnon Lotem as a possibility).

Wilson's Warbler feeding it's Cowbird chick  "offspring"

Why are you feeding this monster? (by Alan Vernon, on Flickr)

The work on trade-offs in this paper provide a simple and intuitive model for the action of brood parasites across a wide variety of situations, and then back it up with empirical data that demonstrate this trade-off in action.  It’s hard to ask for more from a paper!  Of course, as with every paper you’ll ever read, “more research is needed” (we have to say that, or we’re straight out of a job, aren’t we).  It wil be interesting to see if this trade-off does actually hold in other species, and combining the principles in this paper with a phylogenetic analysis would make for a fascinating approach. In the meantime, though, if you’ve read this far I’d urge you to take the lesson of this paper to hear and learn to look for the trade-offs inherent in many biological systems.  As a guiding principle of biology, I guarantee that you’ll see it almost everywhere you look.

Tagged , , ,

Gay zebra finches, oh my. Oh, wait…

Taeniopygia guttata (Zebra finch)

Image via Wikipedia

I’ve seen this paper about strong homosexual pair bonding in zebra finches pop up in a couple of places around the web, but it only really caught my eye when I read Carin Bondar’s somewhat breathless report on the matter entitled “The astounding strength of homosexual bonds in Zebra Finches: Ladies need not apply…”.  In essence, the researchers discovered that when you manipulate the sex ratio of zebra finch groups to be male-biased, male pair bonds form that display all of the same behaviours that female-male pair bonds do, and that when females are later reintroduced to these homosexual pair bonds, the male pair-bonds don’t break up.

It’s an interesting paper, and the findings are, well, pretty cool.  But I have to disagree – respectfully – with Dr. Bondar’s assessment of the startling nature of these results.  First, given that zebra finches tend to mate for life anyways, the finding that male-male pair bonds are strong shouldn’t come as a surprise if you think mechanistically.  In fact, I think it would have been a lot more surprising if the male-male bonds had been of a different quality;  if you think through the evolutionary implications, having a different mechanism for male-male as opposed to male-female bonds would imply that selective pressures on these types of bonds was different for some reason, and would really beg the question of why.  Instead of a single ‘mating’ mechanism (a combination of hormones and neurobiology among other things, which I’ll touch on again in a moment), this ‘conditional’ pair bonding would require either a single mechanism with an unintended consequence, or two separate mechanisms, one for male-male bonds and one for male-female.  That’s not out of the question, certainly;  many potential explanations for same-sex sexual behaviour in animals imply such mechanisms.  But to me, having a life long pair bond with females and then an entirely separate short-term pair bonding mechanism for male-male interactions would need explanation.  Indeed, as Dr. Bondar’s own blog post notes, “homosexual couples both COURTED and COPULATED with each other”;  even if homosexual pairings are adaptive (as they might well be!), it seems odd to waste even a little energy on copulation and suggests a single mechanism or set of mechanisms at work.

Second, it was already established that there are both hormonal and social / developmental mechanisms affecting same-sex preferences in zebra finches;  in particular, Elizabeth Adkins-Regan did a lot of work from the late 90s onwards on both of these mechanisms (and her student, James Goodson, has done a lot of great follow-up work on mapping the endocrinology and neurobiology of social behaviour in estrildid finches).  The finding in the article by Elie et al. that biased sex ratios promote homosexual pair bonds is interesting, but I wonder how different it is from the social deprivation work by Adkins-Regan and her collaborators.

Don’t get me wrong:  this is a cool article.  It deserved to be published, and it seems to make a couple of important contributions- exploring and quantifying the strength of these bonds was a worthwhile task, and the evidence it provides for the “social partner hypothesis” is worth looking at.  But the media has, as per usual, gotten most of the story wrong here (for instance, the BBC Nature story made it sound like the paper was the first to establish same-sex bonds in zebra finches – <sigh>), and while I share Dr. Bondar’s interest in the results, I don’t think that they’re nearly as shocking as she does.

As a postscript to this:  at the end of her article, Dr. Bondar says:

 However, long term studies will shed light on whether males will seek out females for the sole purpose of genetic propagation outside of their homosexual partnerships.  For the sake of their evolutionary future I hope they do :)

I’m not aware of anyone having tested this specifically.  But it’s been known for a long time that zebra finches engage in a fair amount of extra-pair copulating (i.e. they’re socially monogamous, but not sexually monogamous), so I would expect that the males are stepping out to enhance their reproductive fitness.

Tagged , ,