Predicting family dynamics in social vertebrates

1. Predicting family dynamics in social vertebrates 鄭先祐 (Ayo) 國立台南大學 環境生態研究所

2. Family dynamics in social vertebrates • 10.1 The changing scope of cooperative breeding research • 10.2 Ecological constraints and the formation of family groups • 10.3 Kinship and the tendency to cooperate • 10.4 Conflicts with changing family composition • 10.5 Conflict over who reproduces • 10.6 The myth of the stable family? • 10.7 Toward a unified evolutionary social theory • Appendix Evolutionary predictions of living within family kin groups Family dynamics

3. Family definition (家庭的定義) • The definition of families is where offspring continue to interact, into adulthood, with their parents. • Simple family, only a single and female group members breed, while • Extended families, two or more group members of one ore both sexes reproduce. • The presence of a breeding male is not essential to the definition of a family. (biparental, matrilineal母系的) • Intact families, the original breeders are still the reproductive, and • Replacement (or step-) families, a breeder has been replaced. Family dynamics

4. 10.1 The changing scope of cooperative breeding research • 合作養育的行為 occur in roughly 3% of bird and mammal species. 倘若野外研究愈多，這個比率可以再加倍。 • 於1978年的問題， • Did ‘helpers’ really contribute significant assistance to the breeders that they attended? • If they did, 這樣的行為是如何演化出來的？ • 於1984年的問題， • The most common form of group found was that of grown offspring helping their parents to rear younger siblings. • Why did offspring remain with their parents? Family dynamics

5. 第一個問題，可用 ecological constraints 解釋。 • Offspring stayed home when opportunities for successful dispersal and independent breeding were ‘constrained’. • 第二個問題，it turned out that helpers themselves benefited in several additive ways by their helping actions. • They increased their own probability of becoming breeders in the future. • They increased their inclusive fitness by helping to rear close genetic relatives. Family dynamics

6. The early 1980s, reproductive skew theory • In the cooperative societies genetic conflicts of interest are inevitable. • Competition will exist between group members over who breeds and who does not. • A general theory of such conflict and its resolution, now termed reproductive skew theory. Family dynamics

7. By 1991 • The original paradox of cooperative breeding largely disappeared with the widespread confirmation that • Helpers frequently do improve their chances of becoming breeders by staying at home and helping temporarily • They frequently do obtain large indirect genetic benefits by helping to rear collateral kin (Emlen, 1991) Family dynamics

8. 目前的研究 • The vast majority of birds and mammals that exhibit cooperative breeding do live in multigenerational family groups. • Families provide an excellent arena for developing and testing evolutionary social theory. • By focusing on families one seeks similarities, rather than differences, among cooperative species. • Focusing on the family structure of many animal societies highlights parallels with the early social organization of our own species. Family dynamics

9. 10.2 Ecological constraints and the formation of family groups • In most organisms, young disperse from their area of birth well before or at least by the age of sexual maturity. • If offspring and parent come into contact later in life, they show no signs of recognition or preferential interaction with one another. • 於multigenerational families, offspring remain in association with their parent(s) beyond the age of sexual maturity and, commonly, throughout their lifetimes. • The key to understanding the evolution of families is understanding delayed dispersal. Family dynamics

10. Why should a growing offspring postpone its dispersal? • Most mature birds or mammals that remain in their natal group do not reproduce; their breeding is suppressed by their more dominant parents. • This is an automatic cost to saying home • Some researchers have emphasized the importance of the constraints on leaving; others the benefits of staying home. • There are very few ‘vacancies’ for dispersing individuals, or that the vacancies are of poor quality. Family dynamics

11. Economic model of family formation • Delayed breeding occurs when the production of mature offspring exceeds the availability of acceptable opportunities for their independent reproduction • Under such circumstances, some offspring must postpone personal reproduction until acceptable breeding opportunities arise and they are able to successfully compete to obtain them • Families will form when such waiting is best done at home. Family dynamics

12. Acorn woodpeckers, Melanerpes formicivorus • Live in groups of two to 12 individuals and typically occupy permanent, year-round territories in the American Southwest. • High-quality territories are in short supply, and most offspring become reproductives by weiting for an established breeder on an existing territory to die, and then successfully competing to fill the breeding vacancy. (Fig. 10.1) Family dynamics

13. Fig. 10.1 (a) Ecological constraints and family formation in acorn woodpeckers (a) the proportion of yearlings that remain at home, plotted as a function of the severity of territorial shortages. Family dynamics

14. Fig. 10.1 (b) the likelihood that yearlings stay at home, plotted as a function of the quality of their natal territories. Family dynamics

15. Superb fairy wren(鷦鷯), Malurus cyaneus • Live in southeastern Australia in families consisting predominantly of parents and grown sons. • Shortages of both territories and mats (females) have been suggested as possible constraints to independent breeding. • By removing breeding males from nearby territories they created breeding vacancies, Thirty-one of 33 mature sons left home to fill the newly created breeding vacancies. Family dynamics

16. The Seychelles warbler, Acrocephalus sechellensis • Is a formerly endangered species whose range is restricted to a few small islands north of Madagascar. • In 1960, when the population consisted of just 26 individuals, habitat restoration programmes were implemented. • Over the following 30 years, the population grew impressively. • No family groups were reported until 1973, roughly the time at which all suitable breeding habitat became occupied (Fig. 10.2a) Family dynamics

17. Fig. 10.2 Ecological constraints and family formation in Seychelles warblers (a) the number of individuals and occupied territories on Cousin island between 1959 and 1990. Family dynamics

18. Fig. 10.2 (b) the likelihood that yearlings stay at home, plotted as as function of the quality of their natal territories. Family dynamics

19. 10.3 Kinship and the tendency to cooperate • Families are fundamentally different form other forms of social groupings because they form by the retention of grown young with their parents. • Families are comprised primarily of close genetic relatives. • Inclusive fitness theory • Kin selection has long been hypothesized to be a selective factor favouring the evolution of cooperative breeding. Family dynamics

20. 合作養育 和multigenerational family group • There 112 species of birds and 63 species of mammals (excluding primates) reported to live in multigenerational family groups. • Of these, fully 96% of the birds and 90% of the mammals exhibit cooperative breeding. • Fully 88% of the birds and 95% of the mammals that breed cooperatively live in multigenerational family groups (Emlen, 1995) • 絕大多數，都是有明顯的kin favouritism • 已知只有一種例外，Maxican jay, Aphelocoma ultramarina, (Brown and Brown, 1990) Family dynamics

21. White-fronted bee-eaters (birds) • Live in extended family groups in which up to four pairs may breed simultaneously. • Helpers are non-breeding individuals that join one of the active nests and aid in incubation as well as nestling and fledgling care. • Only 50% of the non-breeders become helpers; the rest sit out the season as non-participants. • Kinship proved to be a strong predictor (Fig. 10.3) • They preferentially help the breeding pair to whom they are most closely related (94% of 115 cases) Family dynamics

22. Fig. 10.3 Data are presented as dyadic comparisons of nest choices plotted according to the helper’s relatedness to the recipient nestlings. 親緣相關係數 Family dynamics

23. Incest avoidance • Incestuous matings between close kin have deleterious genetic consequences in most normally outbreed species. • 因此於Family group, 應該有 inbreeding avoidance mechanisms. • Family dwelling species provide an excellent testing ground for incest avoidance predictions because mature offspring remain in close social contact with their parents and siblings throughout subsequent reproductive episodes. • Incestuous matings within families are statistically rare. • 但是 incest avoidance is not universal among vertebrates. Family dynamics

24. 10.4 conflicts with changing family composition • The death, divorce or departure of a breeding parent, and its replacement from outside the group, will alter the basic genetic and dominance structure of the family unit. • As a result, 家庭組成改變 (replacement families)，情況將會不同。 • A replacement mate will typically be unrelated to extant family member. 如此就沒有 incest restrictions. • Son could mate with its stepmother, daughter could mate with its stepfather. Family dynamics

25. Stripe-backed wrens, Camphylorhynchus nuchalis • Live in nuclear families of two to seven individuals in the savannas of Venezuela. • Piper and Slater (1993) contrasted the behaviour of sons in intact versus replacement families. • Sons displayed no sexual interest in their mothers, but they frequently engaged in courtship activities with their stepmothers. • When sons attempted to consort sexually with their stepmothers, fathers upped their mate-guarding behaviours and became increasingly aggressive toward their sons. (Fig. 10.4) Family dynamics

26. Fig. 10.4 Differences in sexually related behaviours within intact (open bars) and replacement (shaded bars) families of stripe-backed wrens. Family dynamics

27. White-fronted bee-eaters • extended family • Male offspring pair with unrelated females but bring their mates home to breed within their natal family groups. • Sons show no sexual interest in their mothers but brothers do attempt sexual activity with their sisters-in-law and fathers occasionally copulate with their daughters-in-law. Family dynamics

28. Infanticide • Replacement mates are not expected to invest substantially in dependent young remaining from previous breedings because they are genetically unrelated to such offspring. • 倘若照顧這些小孩的代價過高，infanticide 的情況就有可能發生。 • This point has been repeatedly confirmed in studies of family-dwelling rodents, carnivores and primates, as well as in many species of birds. Family dynamics

29. Replacement families • Offspring in replacement families also suffer a reduction in the indirect fitness benefit. • The offspring will share only 25% of their genes with future half-siblings, in contrast to the 50% shared with full-siblings. • 因此，percentage of helper 應該會下降。 • Florida scrub jay and Seychelles warbler (Fig. 10.5) Family dynamics

30. Fig. 10.5 The likelihood that non-breeding family members will serve as helpers, plotted as a function of family type. (a) Florida scrub jay Family dynamics

31. Fig. 10.5 The likelihood that non0breeding family members will serve as helpers, plotted as a function of family type. (b) Seychelles warbler Family dynamics

32. Replacement families • Red-cockaded woodpeckers and stripe-backed wrens, in contrast, did not alter their feeding rates when provisioning full-versus half-siblings. • Replacement families are predicted to be less stable than intact biological families. • Instability, in terms of increased dispersal tendencies of mature offspring or in terms of increased separation rates of re-paired breeders. Family dynamics

33. Fig. 10.6 Generalized genealogical diagrams of two forms of replacement family (a) A stepfamily formed from a formerly intact nuclear family when, following the death of the original breeding female the male parent takes a new mate and reproduce again.(b) A ‘blended’ family in which two formerly nuclear families, each with offspring, join when the widowed male parent from one pairs with the widowed female of the other. Family dynamics

34. 10.5 Conflict over who reproduces • The dominant pair monopolizes breeding • Subordinates would often increase their fitness if they could become reproductive themselves. • They are two ways a subordinate may become a breeder within its natal group. • It can simply replace the dominant breeder • It can share reproduction alongside the dominant Family dynamics

35. 10.5 Conflict over who reproduces • 10.5.1 The benefit of group-living • 10.5.2 The probable success of attempted independent reproduction • 10.5.3 kinship • 10.5.4 social dominance and fighting ability Family dynamics

36. 10.5.1 the benefit of group-living • This provides the adaptive explanation for why dominant individuals share breeding at all. • The greater the magnitude of the group-living benefit realized by the dominant, the greater the potential leverage wielded by the subordinate. Family dynamics

37. 10.5.2 The probable success of attempted independent reproduction • Consider the case where the chance of successful independent reproduction is near zero • In such instances, parents have extreme leverage because an offspring has little option but to remain at home. • The situation changes when opportunities for independent reproduction improve. Family dynamics

38. 10.5.3 kinship • Genetic relatedness between group members is the third critical parameter. • A dominant breeder 會與其近親分享breeding? • No. • 通常是基因型差異較大的，才需要分享。 • This prediction has been confirmed in numerous species. Family dynamics

39. Kinship consideration also predict that reproduction will be shared more equitably in sibling-sibling associations than in parent-offspring groupings. • Reproductive sharing generally will not be favoured between mothers and daughters (or fathers and sons). Family dynamics

40. 10.5.4 social dominance and fighting ability • Dominance hierarchies exist in most vertebrate families. • Dominant individuals are always at risk of losing their top position. • The costs of challenges can be high for both participants. • When the risk is sufficiently great, it will become advantageous for the dominant to share reproduction as a ‘peace incentive’ with its potential challenger. Family dynamics

41. 10.6 the myth of the stable family? • Family structure is dynamic. • Predictable changes should occur: • As the benefits of large group size wane; • As ecological opportunities for independent breeding increase or decrease; • As breeder deaths and replacements, as well as immigrations alter family composition; • As the social dominance of individual changes with age and experience. Family dynamics

42. 10.7 toward a unified evolutionary social theory • The building blocks of a unified science, as described in this chapter, consist of ecological constraints theory, kin-selection theory, social dominance theory and reproductive skew theory. • Cooperatively breeding species have played, and will continue to play, a pivotal (樞軸的) role in the development of evolutionary social theory. Family dynamics

43. Appendix Evolutionary predictions of living within family kin groups • Family groupings will be inherently unstable. • Families that control high-quality resources will be more stable than those with lower quality resources. • Assistance in rearing offspring will be more prevalent in family groups than in otherwise comparable groups comprised of non-relatives. • Assistance in rearing offspring will be expressed to the greatest extent between those family members that are the closest genetic relatives. • Sexually-related aggression will be less prevalent in family groups than in otherwise comparable groups comprised of non-relatives. Family dynamics

44. Breeding males will invest less in offspring as their certainty of paternity decreases. • The loss of a breeder will result in family conflict over the filling of the resulting reproductive vacancy. • Sexually-related aggression will increase after the re-pairing of a parent. • Replacement breeders (step-parents) will invest less in existing offspring then will biological parents. • Non-reproductive family members will reduce their investment in future offspring following the replacement of a closely related breeder by a more distantly or unrelated individual. Family dynamics

45. Replacement families will be inherently less stable than biologically intact families. • Reproduction within a family will become increasingly shared as the severity of ecological constraints decreases. • Reproduction within a family will become increasingly shared as asymmetry in social dominance between potential cobreeders decreases. • Reproduction within a family will be shared more equitably when the potential cobreeders consist of siblings than when they consist of parent and grown offspring. • Reproduction will be shared most with those family members to whom the dominant breeders are least closely related. Family dynamics

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