Evolution of Stable Biparental Care

Question 1

Evolution of stable biparental care

Answer 1

Biparental care is widespread in animals, particularly in certain groups, such as birds, but also in other taxa, such as frogs, fish, burying beetles and humans. However, there is inevitable conflict between parents over the provision of biparental care and in this lecture we will examine theoretical solutions for the evolution of stable biparental care and empirical tests of theoretical predictions.

Question 2

1. Why is the evolution of biparental care problematic?
   Parental care is costly and life history theory predicts that current investment should be traded off against future survival and reproduction.

Answer 2

In systems with biparental care, each parent bears the costs of their own investment individually, while the benefits of their investment (i.e. offspring fitness) are shared. Thus, each parent should try to increase their own fitness by reducing their reproductive costs at the expense of their partner. This is a particular case of the general phenomenon known as the ‘tragedy of the commons’. This is a classic example of a situation where game theoretic reasoning allows us to understand the ‘investment game’ that is played out between parents.

Question 3

2. Theoretical solutions
   A series of theoretical models have explored parental investment games.
   Houston & Davies (1985) proposed a ‘sealed bid model’ in which a parent’s best response to the effort of a partner is allowed to evolve through time. Each parent has an optimal response to their partner’s effort, and an ESS may be reached at which there is stable investment by both parents (although other outcomes – i.e. uniparental care by either sex - are also possible). As suggested by the sealed bid model, an individual’s effort may be repeatable across different breeding attempts (e.g. Nakagawa et al. 2007) and in a couple of cases has been shown to be heritable, i.e. partly genetically determined (e.g. MacColl & Hatchwell 2003). However, in general, parents are able to adjust their effort according to circumstances (brood size, nestling age, conditions, etc), so that care may vary in real (behavioural) time, making the notion of a ‘sealed bid’ less likely.

Answer 3

McNamara et al. (1999) proposed a ‘negotiation model’ in which parents negotiate with each other over their optimal investment in behavioural time, the negotiation rules that are used by parents being allowed to evolve over time. This model is more inclusive of potential influences on parental effort and recognizes that in many cases parents do indeed adjust the rate at which they provision offspring in relation to various factors.
Importantly, both models share the general prediction that: stable biparental care evolves when one parent compensates incompletely for a reduction in effort by their partner. That is, if one parent reduces their effort (perhaps with the goal of exploiting their partner by getting them to work harder), then the partner should increase their effort a little, but not enough to compensate for the first parent’s reduced effort. Thus there is a reduction in total effort and a cost to offspring (and hence parental) fitness.

Question 4

Empirical studies
This general prediction of incomplete compensation has been empirically tested many times, almost entirely in field studies of various biparental bird species, using a variety of approaches to manipulate one parent’s effort and measure their partner’s response.
(a) Removal experiments
If one parent is removed, does the other show partial compensation? Yes, often. e.g sunbirds (Markman et al. 1996).
(b) Handicapping experiments
If one parent is handicapped (by adding weights or tying/clipping feathers) so that they reduce their effort, does the other show partial compensation? Again, yes, in some cases, although in others, compensation appears to be complete, e.g. European starlings (Wright & Cuthill 1990), or non-existent, e.g. blue tits (Slagsvold & Lifjeld 1990).
(c) Testosterone experiments
Males treated with testosterone reduce their care; do females compensate? Again, yes, in some cases, although compensation may again be complete, e.g. dark-eyed juncos.
(d) Meta-analysis
A meta-analysis of 54 experimental studies (Harrison et al. 2009) found general support, on average, for the prediction of incomplete compensation for reduced effort by one parent. But, the results of these experiments have been extremely variable, resulting in partial compensation (as predicted), but also full compensation, no response, or a variable response according to sex.
There are likely to be two main reasons for this variability:

Answer 4

Experimental methodology – removal of a parent does not allow for negotiation, the partner being effectively ‘widowed’. Handicapping and testosterone experiments may change a partner’s perception of the quality of the manipulated parent so the response may be influenced by that change in perception, rather than the change in their effort. Finally, if an individual is already working at full capacity, they may be unable to increase their effort further.

Information – the models described above assume that parents have perfect information about their partner’s effort and the needs of the brood. This may not be true.
Johnstone & Hinde (2006) proposed the ‘information model’, a version of the negotiation model, which recognizes that parental information about brood need may be incomplete. Here, a parent may rely on cues provided by their partner to assess the effort required, or they may integrate information from the brood and their partner. This could explain the variability observed in responses to experimental manipulations.
(e) Playback experiments
This model is supported by results from the few playback experiments conducted so far. When one partner is asked to work harder by playing back extra begging calls to them, their partner usually matches that response (the opposite result to the predicted compensation), e.g. great tits (Hinde 2006) and long-tailed tits (Meade et al. 2011).

This outcome could arise if the mode of negotiation between parents is alternation of provisioning visits (or reciprocal care). There is some very limited evidence that this may indeed be the case, e.g. great tits (Johnstone et al. 2014) and long-tailed tits (Bebbington & Hatchwell 2016).

Question 5

Conclusion
Although there is general support for theoretical predictions of partial compensation in biparental care, there is much variation among studies.

Answer 5

Understanding is likely to be improved by further consideration of the information available to parents and of the process of parental negotiation.