Long-tailed Tits - Cooperative Breeding Flashcards
Long-tailed tits Aegithalos caudatus are one of very few UK bird species that breed cooperatively. Their social system makes them ideal for asking functional and mechanistic questions about the causes and fitness consequences of cooperative behaviour.
The aims of this lecture are to describe: (a) the long-tailed tit’s social system, (b) the fitness consequences of helping and the role of kin selection, (c) the mechanism of kin recognition, (d) the processes generating interactions among kin, and (e) the factors that constrain independent breeding and cause helping.
(a) Cooperative breeding in long-tailed tits
Since 1994, long-tailed tits have been studied in a 2.5 km2 area of the Rivelin Valley, just outside Sheffield. A population of c.100-150 individually marked adults is monitored each year, all breeding attempts are found, and cooperative behaviour observed.
Blood samples are taken for molecular genetic analysis so that the relatedness of all members of the population can be determined and a pedigree can be produced. This is among the longest studies of any cooperative species, and probably the longest in terms of the number of generations followed because they are relatively short-lived.
During the non-breeding season, long-tailed tits live in flocks of 10-20 birds. Dispersal (especially of young females) occurs during this period so that flocks are composed of both kin and non-kin. In March, flocks break up and all birds pair up monogamously. There is a 1:1 sex ratio, so there are no non-breeders or helpers at this time of year. Each pair makes their own nest (a complex structure) and females lay a clutch of c.10 eggs.
If all goes well, after c.15 days of incubation, the brood hatches and nestlings are fed for 16-17 days, when they fledge and form a family flock. They are single-brooded, so if a pair manage to raise a brood, they won’t try to breed again until the following year.
However, most (c.75%) of all breeding attempts fail, generally due to nest predators. A pair may then attempt to breed again. But, if nest failure occurs after early May, instead of re-nesting, failed breeders abandon breeding for that year (MacColl & Hatchwell 2002 American Naturalist 160:186-194).
Some failed breeders (especially males) then move to the nest of another pair to become helpers; the others just hang out doing not very much. About half of all broods have helpers, typically 1-3, but up to 8 at a single nest. Helpers assist the pair by feeding the brood both before and after fledging. They generally stay with the subsequent flock through the following winter (see Hatchwell et al. 2004 Behavioral Ecology 15: 1-10 for further details).
(b) Fitness consequences of helping
Indirect fitness benefits – Observations show that helpers usually help at a nest belonging to a relative. This could happen by chance, but in an experiment, when failed breeders were given a choice between a nest belonging to kin and non-kin they almost always chose that belonging to kin (Russell & Hatchwell 2001 Proceedings of the Royal Society B 268: 2169-2174).
Moreover, helpers work harder when they are more closely related to the helped brood (Nam et al. 2010 Proceedings of the Royal Society B 277: 3299-3306). Finally, helpers have a substantial positive effect on the probability that fledglings survive to adulthood, i.e. recruit into the breeding population (Hatchwell et al. 2004, ref above). In addition, when male breeders have helpers, they reduce male breeders’ cost of reproduction so they are more likely to survive to the following year than breeders without helpers (Meade et al. 2010 Journal of Animal Ecology 79: 529-537). Therefore, helpers prefer to help kin and gain indirect (kin-selected) fitness benefits from their helping behaviour.
Direct fitness benefits – By contrast, we have no evidence that helpers enhance their future survival or reproduction relative to non-helpers (Meade & Hatchwell 2010 Behavioral Ecology 21: 1186-1194).
Neither do helpers gain any reproductive success in the current brood because there is no brood parasitism and a low rate of extra-pair paternity (Hatchwell et al. 2002 Animal Behaviour 64: 55-63). Thus, there are no direct benefits of helping.
Partitioning the direct and indirect components of inclusive fitness – Using data on Lifetime Reproductive Success, we can partition inclusive fitness into its direct and indirect components.
This shows that most birds that reach adulthood achieve zero fitness, but of the minority that do, a substantial proportion of inclusive fitness (about 20-25%) is gained indirectly, and especially by individuals who have achieved no direct fitness (MacColl & Hatchwell 2004 Journal of Animal Ecology 73: 1137-1148).
Testing Hamilton’s rule – Using information on the benefits of helping (increased productivity and survivorship of helped breeders), the costs of helping for helpers (reduced survivorship and hence future reproductive success), and relatedness (pedigrees and genotyping), we can parameterize Hamilton’s rule.
This analysis shows that helping is costly, and hence altruistic, but these costs are outweighed by the fitness benefits, as predicted by Hamilton’s rule (Hatchwell et al. 2014 Philosophical Transactions of the Royal Society B 369: 20130565).
(c) Processes generating kin-structured populations in which kin selection can operate
Kin selection can operate only if there are frequent interactions among kin, so what processes generate the kin structure we see in long-tailed tits (Leedale et al. 2018 Molecular Ecology 27: 1714-1726)?
Limited dispersal driven by constraints is the usual explanation, but although most long-tailed tits don’t disperse far, it is not unusually limited compared to non-cooperative species, and they don’t stay in their nuclear family group as many cooperative species do (Sharp et al. 2008 Oikos 117:1371-1379). However, when long-tailed tits disperse, they often do so with relatives, so dispersal does not necessarily result in birds moving away from their relatives, so kin interactions can occur post-dispersal (Sharp et al. 2008 Proceedings of the Royal Society B 275: 2125-2130).
In addition, the long-tailed tit’s unusual demographic/life history traits seem to be a major contributor to population kin structure. The very high rate of nest predation means that a relatively small number of pairs reproduce successfully, but each brood produces a lot of related fledglings from which a large proportion of next year’s recruits are drawn. Thus, there is a small effective population size.
This contrasts with more typical avian life histories (e.g. great tits) where many pairs are successful, producing many fledglings, of which relatively few survive to become breeders; i.e. there is a large effective population size. This simple difference in the timing of offspring mortality has a profound effect on the emergent population kin structure (Beckerman et al. 2011 Behavioral Ecology 22: 1294-1303).
(e) Constraints on independent breeding?
One approach to investigating the constraints driving cooperative breeding is to study the same population across many years and then ask what ecological or life history factors co-vary with helping behaviour. For long-tailed tits, we predicted three factors would be important:
Nest predation rate – If there is little nest predation there will be few potential helpers; if there is a high rate of nest predation there will be few nests available to be helped. Therefore, helping was predicted to peak at intermediate levels of nest predation when there are both potential helpers and potential recipients.
Length of the breeding season – In a short season there will be little time to have multiple attempts to raise your own brood, whereas in a long season each pair can have multiple attempts. Therefore, helping was predicted to be negatively correlated with the length of the breeding season.
Relatedness – If the presence of kin is necessary for failed breeders to become helpers, then helping was predicted to increase as average population relatedness increased.
As predicted, the prevalence of helping in the population peaked at intermediate levels of nest predation, with low prevalence at low and high rates of predation. Secondly, the intensity of helping decreased as the length of breeding seasons increased, again as predicted. In contrast, there was no significant relationship between helping and relatedness, probably because it is the kinship of individuals that matter rather than relatedness at the level of the population (Hatchwell et al. 2013 Journal of Animal Ecology 82: 486-494).
This result exemplifies the difficulty of explaining the occurrence of cooperative breeding across species – predation is a novel driver of helping in cooperatively breeding birds, as is length of the breeding season, therefore adding to the diversity of constraints identified in single species studies. Nevertheless, it would be surprising if the same factors did not correlate with helping in similar cooperative breeding systems.
Conclusion
- Long-tailed tits have a kin-selected cooperative breeding system (indirect, but no direct fitness benefits).
- Inclusive fitness can be quantified, partitioned into its direct and indirect components, and Hamilton’s rule tested thereby demonstrating the importance of kin selection in this system.
- The kin-structured populations required for kin selection to operate results from limited (but not delayed) dispersal, coordinated dispersal of kin, and a life history that results in a small effective population size.
- Helping is driven by nest predation and short breeding seasons, both of which reduce the opportunity for successful independent reproduction. This is consistent with Emlen’s Ecological Constraints Hypothesis for the evolution of cooperative breeding.
