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.

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