Mothers and Others

by Sarah Blaffer Hrdy

  32. Wilson 1975; Hölldobler and Wilson 1990:164.

  33. Hölldobler and Wilson 1990.

  34. See O’Riain, Jarvis, et al. 2000 for first demonstration of increased body size in breeding mole rats. See Holmes et al. 2007 for differences in brain cells.

  35. Wilson and Hölldobler 2005.

  36. See esp. Griffin and West 2003 for a meta-analysis of the relation between kin discrimination and the benefits from helpers among vertebrates.

  37. Davies 1992.

  38. Rubenstein 2007.

  39. See Jennions and Macdonald 1994 for an overview and for hyenas; Marlowe 1999b for Hadza.

  40. Double and Cockburn 2000; see also Cockburn, Osmond, et al. 2003.

  41. Dunn et al. 1995.

  42. Mulder and Langmore 1993.

  43. Mulder et al. 1994.

  44. Emlen (1982, 1991) is the principal architect of this ecological-constraints hypothesis. See also edited volume by Koenig and Dickinson (2004).

  45. Arnold and Owens 1998.

  46. Queller 2006:42; West-Eberhard 1975.

  47. West-Eberhard 1986.

  48. Reeve and Gamboa 1987; see also Wenseleers and Ratnieks 2006.

  49. Cockburn 1998:161; Boland et al. 1997.

  50. Hughes and Boomsma 2008.

  51. Emlen et al. 1995:157.

  52. Dierkes et al. 1999; Barlow 2000. In addition to having been observed in these fish, alloparental care was also recently reported in reptiles, in skinks belonging to the family Scincidae (O’Connor and Shine 2002).

  53. Helpers “pay to stay” by preemptive appeasement (Bergmuller and Taborsky 2005); see also Kokko et al. 2002.

  54. Holmes et al. 2007; Russell, Carlson, McIlrath, et al. 2004.

  55. Clutton-Brock et al. 1998; Clutton-Brock 2002.

  56. Young and Clutton-Brock 2006.

  57. See Digby 2000 for the best available review.

  58. Suppressed ovulation is not known to occur in humans; however, enforced wet-nursing has been widespread at different times and places, suggesting that some humans may once again have converged through cultural means on behaviors similar to evolved adaptations in other cooperatively breeding mammals (e.g., Hrdy 1999, ch. 14).

  59. For example, see Solomon and French 1997.

  60. Heinsohn 1991.

  61. See Emlen 1991 for classic formulation of relationship between cooperative breeding and saturated habitats.

  62. See Koenig and Stacey 1990 for food storage.

  63. See Hrdy 1999:155–156, 191–193 and references therein.

  64. For example, Whitehead and Mann 2000; Boran and Heimlich (1999) speculate that some cetacean traditions are deliberately taught.

  65. To date, the strongest evidence for the correlation between social integration and maternal reproductive success comes from long-term study of savanna baboons at Amboseli (Silk et al. 2003; see also Silk 2007).

  66. For formal theory behind this idea, actually worked out long ago by hunter-gatherers themselves, see Fehr and Fischbacher 2003; Bowles and Gintis 2003.

  67. Known as the life-history hypothesis (Arnold and Owens 1998).

  68. Cockburn 1996; Russell 2000; Ekman and Ericson 2006.

  69. Cockburn 2006.

  70. Cockburn 2006.

  71. For example, in a controlled study of 45 species of African starlings, Rubenstein and Lovette (2007) found that cooperative breeding was more likely to evolve in those living in semi-arid savanna habitats with unpredictable rainfall than in either deserts or forest habitats.

  72. Marshall 1976; Lee 1979.

  73. Ligon and Burt 2004:6; see also Jamieson 1991; West-Eberhard 1988b.

  74. Whereas cooperative breeding is found only 4 percent of avian clades with precocial young, it is found in 11 percent of those with altricial young (Cockburn 2006).

  75. Ligon and Burt 2004:21.

  76. See Kilner and Johnstone 1997; Kilner et al. 1999.

  77. Russell, Langmore, et al. 2007.

  78. Toth et al. (2007) used the sequenced genome of the eusocial honeybee (among whom workers but not queens provision) as their baseline for identifying genes in the genome of Polistes workers, foundresses, and queens, all of which are involved in foraging and reproduction. Genomes of the late-stage Polistes queens more nearly resembled those of honeybee queens.

  79. West-Eberhard 2003. Chapter 11 of her book is specifically devoted to such “trait loss.” The quotation comes from p. 10. As she points out, deletions and other sorts of evolutionary change in developmental sequences can all be called “heterochrony” (the term preferred by Toth et al.) because all involve changes in the timing of expression (upward and downward regulation of gene activity).

  80. West-Eberhard 2003, quotation from p. 223; see also 1988b.

  81. For non-hunter-gatherer examples see Cashdan 1990; Hrdy 1981a, ch. 7; Strassmann 1997; Strassmann and Hunley 1996; and hopefully more to come.

  82. Boyette 2008 and personal communication; Crittenden and Marlowe 2008; on children fostered in, see Hrdy 1999, ch. 11.

  83. Paula Ivey Henry, personal communication, May 10, 2008.

  84. Betzig 1986; Betzig is preparing a synopsis of the human potential for creating societies with extreme reproductive skews (personal communication 2008).

  85. For overviews of extensive literatures on wet-nursing through history see Hrdy 1997, 1999, chs. 12 and 13 and references therein. For an early treatment of this puzzling disconnect between extensive empirical documentation of female-female competition in other primates contrasted with a dearth of such evidence in the human literature, see Hrdy 1981a:129–130.

  86. Foster and Ratnieks 2005; Cant and Johnstone 2008.

  7. BABIES AS SENSORY TRAPS

  1. Lacey 2002.

  2. Brennan 2006.

  3. Singer 2007.

  4. Wisenden and Keenleyside 1992.

  5. Costa 2006.

  6. See Fleming et al. 1994 for the original experiments. See Ferris et al. 2005 for replication and overview of relevant experiments.

  7. Martel et al. 1993; Keverne 2005.

  8. Strathearn, Li, et al. 2007.

  9. Zahed et al. 2007.

  10. Wynne-Edwards and Timonin 2007 and references therein.

  11. Whereas pregnant langur monkeys (Semnopithecus entellus) are highly motivated to take and hold infants (Hrdy 1977a, Tables 7.4 and 7.8), common marmoset (Callithrix jacchus) allomothers in the later stages of pregnancy are surprisingly infanticidal (Bezerra et al. 2007; Saltzman et al. 2008, esp. Fig. 2B).

  12. See Roberts et al. 1998 for one of the few early papers to specifically advocate looking at alloparents; also Carter et al. 2005; Bridges 2008.

  13. Olazábal and Young 2006.

  14. These include the medial preoptic area, medial forebrain bundle, and trigeminal area. See Gregg and Wynne-Edwards 2005 for pioneering overview of this literature.

  15. Plenary address, Human Behavior and Evolution Society 2003 meeting, Lincoln, Nebraska; the video was made by Marc van Roosmalen.

  16. On placentophagia see Gregg and Wynne-Edwards 2005; Wynne-Edwards and Timonin 2007:6. For more on oxytocin and bonding, see Carter 1998.

  17. Menges and Schiefenhövel 2007; I am also indebted to ethnographers W. Schiefenhövel, James Chisholm, and Victoria Burbank for information about the absence of placentophagia among the Eipo and Australian Aborigines.

  18. Hrdy 1977a, Tables 7.5 and 7.9.

  19. Personal communication, Jeanne Altmann, December 6, 2007.

  20. Hrdy 1976; Silk 1999. When the term “kidnapped” is used for infant-sharing monkeys like langurs, the term refers to a female forcibly taking a new infant from a female belonging to a different troop during intertroop encounters (Hrdy 1977a, ch. 7).

  21. Henzi and Barrett 2002; see p. 915 for quotation. For more on the spider monkey case see Slater et al. 2007.

  22. Seay 1966; Lancaster 1971; Hrdy 1976; Silk 1999.

  23. Altmann, Hausfater, and Altmann 1988:412.

  24. Hrdy 197
7a, ch. 7; Numan 1988.

  25. It would be useful to know if, all other things being equal, primiparas suffer on average less infant mortality in infant-sharing species, but to my knowledge data to test this proposition are not currently available.

  26. See Kringelbach et al. 2008 for further details which involved a technique called magnetoencephalography.

  27. Hurlburt and Ling 2007.

  28. At present, we know more about competition for parental and alloparental attentions in nonhuman than human cooperative breeders (e.g., Hodges et al. 2007 and references therein). Part of the reason is that it is easier to quantify competition in litter-bearing species with same-age littermates. In humans, competition is often between offspring of very different ages and capacities. Sibling competition in particular can involve older versus younger sibs, or even sibs yet to be born (Trivers 1974; Hrdy 1999:460–461ff).

  29. Sumner and Mellon 2003; Isbell 2006. New World howler monkeys appear to be an exception to this rule since they do have color vision. It may be worth noting in this context that at least one species of howler monkeys exhibits moderate amounts of infant sharing and also bears young with distinctive natal coats (Hrdy 1976). This is a topic that cries out for further study.

  30. Discussed in Hrdy 1999, in a chapter entitled “A Matter of Fat.”

  31. See Hrdy 1999, chs. 19–21, for more on the topic of discriminating human mothers and “runaway selection” for plumpness and other traits likely to appeal to mothers.

  32. Gottlieb 2004:329.

  33. Gottlieb 2004:163, 188, and throughout.

  34. Gottlieb 2004:134.

  35. Gottlieb 2004: 95ff., esp. pp. 132, 187–188.

  36. Martins et al. 2007.

  37. For example, Estrada 1982; briefly reviewed in Hrdy 1999:156–161.

  38. For additional information on the practice of “fostering out” see Hrdy 1999:370–376.

  39. Statistics from Child Welfare Information Gateway (www.childwelfare.gov) and from U.S. Department of Health and Human Services (www.hhs.gov).

  40. Silk 1990.

  41. For recent overview of primate infanticide see van Schaik and Janson 2000. In both traditional and industrial human societies, discriminatory treatment of orphans and stepchildren can range from nil or mild (Bledsoe and Brandon 1987; Case and Paxson 2001; Case et al. 2004) to extreme (Chagnon 1990; Daly and Wilson 1999).

  8. GRANDMOTHERS AMONG OTHERS

  1. Fossey 1984; Goodall 1986; Hamai, Nishida, et al. 1992; Harcourt and Stewart 2007; Pusey, Williams, and Goodall 1997; Townsend et al. 2007.

  2. When attacks by a female called Passion on three infants in her community were first observed at Gombe, Goodall (1977) interpreted these “crimes of passion” as pathological behavior. However, sociobiologists immediately recognized the parallels with other species where infanticidal females increase their own, or their offspring’s, access to resources by eliminating other females’ offspring. When cannibalism is involved, the infant itself becomes a resource (Hrdy 1979, 1981a:108–109; Digby 2000 for recent overview). Today, on the order of 5–20 percent of mortality in the first months of life of infants born at Gombe is attributed to infanticide by females (Pusey et al. 2008).

  3. Townsend et al. 2007.

  4. Masayuki Nakamichi, personal communication, April 14, 2008.

  5. Wroblewski 2008.

  6. Nakamichi et al. 2004.

  7. See Thierry 2007 for an up-to-date and comprehensive overview.

  8. Carter 1998; Carter et al. 2001; Bosch et al. 2005; specifically in regard to oxytocin and trust in humans see Kosfeld et al. 2005.

  9. Carter 1998.

  10. Bales et al. 2007; also Bales, Pfeiffer, and Carter 2004; Bales, Kim, et al. 2004. It is impossible also not to acknowledge the psychobiologist Sue Carter, who decades ago urged researchers to pay more attention to oxytocin.

  11. Olazábal and Young 2006, and references therein.

  12. See Knight and Power 2005 for a well-researched overview.

  13. For example, Thiessen and Umezawa 1998; Pinker 1997; Buss 1994a.

  14. For example, Solomon and French 1997; refer back to Chapter 6. I still recall the first lecture I ever gave on humans as cooperative breeders in 1999, when a prominent zoologist in the audience asked, if so, “Why don’t we find reproductive suppression in hunter-gatherers?” His question prompted me to tackle the problem (Hrdy 2002, Part II).

  15. For example, in a recent phylogenetic-cum-behavioral analysis, Rendall and Di Fiore (2007, Fig. 2) highlight the lack of tolerance between Great Ape females.

  16. Ember 1975; Murdock 1967, reviewed in Alvarez 2004.

  17. Ghiglieri 1987; Wrangham 1987; Rodseth et al. 1991.

  18. See such early classics as Darwin 1874; Lévi-Strauss 1949; Tiger 1970.

  19. I am scarcely an unbiased commentator. I vividly recall these times, and some of the early criticisms were my own (e.g., Hrdy 1981a; Hrdy and Williams 1983).

  20. Knight and Power 2005 provide an in-depth historical review of early reactions to the grandmother hypothesis and their background. As a historical note, I was among those convinced early on that apes tended toward patrilocality. I only changed my mind in the course of writing Mother Nature (1999). By 1997 I was sufficiently impressed by the flexibility of hunter-gatherer residence patterns that I sponsored Hawkes et al.’s then still controversial, but by now classic, 1998 paper on the grandmother hypothesis for publication in PNAS.

  21. See Hart and Pilling 1979:124ff for a particularly vivid, if extreme, example; discussed further in Hrdy 2005c.

  22. See Hawkes and Blurton Jones’s (2005) review of this literature, summarizing reasons why they are now convinced that significant numbers of women in the Pleistocene survived into their sixth and even seventh decades.

  23. Gurven and Kaplan 2007:326.

  24. Based on demographic analyses by Nancy Howell in 1976, cited in Hawkes and Blurton Jones 2005; Biesele and Howell 1981.

  25. Judge and Carey 2000; Lahdenperä et al. 2004; Gurven and Kaplan 2007:349.

  26. Williams 1957; quotation from Hamilton 1966. Their ideas were subsequently applied to primates by Hrdy and Hrdy (1976).

  27. I review different versions of the grandmother hypothesis as well as the competing prudent-mother hypothesis elsewhere: Hrdy 1999, ch. 11; see also Voland et al. 2005; Paul 2005.

  28. Information on this last daughter, Furaha, provided by the Jane Goodall Institute, 2007. For background see Pusey et al. 1997.

  29. On the basis of behavioral data alone, prior to the availability of genetic data, a few authors had suggested that Great Ape breeding systems would turn out to be fairly flexible (e.g., Harcourt et al. 1981). However, this hypothesis was not confirmed until collection of hair and discarded wads of chewed leaves made microsatellite genotyping of wild chimpanzees possible (Vigilant et al. 2001; see also Langergraber, Mitani, and Vigilant 2007).

  30. Harcourt and Stewart 2007.

  31. Alvarez 2004; Marlowe 2004, whose analysis builds on and supports that of Alvarez.

  32. Quotations from Pinker 1997:477 and Pinker 2002:323.

  33. Alvarez 2004; Marlowe 2004; Blurton Jones, Hawkes, and O’Connell 2005a, 2005b provide a specific case study; see also Ember 1975, 1978; Ember and Ember 2000.

  34. Loeb 1926, cited in Alvarez 2004, Table 18.1.

  35. From Riddell 1978, cited in Alvarez 2004, Table 18.1.

  36. Wives lobby for sisters as co-wives in many polygynous societies (Irons 1988). See Chisholm and Burbank (1991) for a prescient discussion of the difference between “sororal polygyny,” which is often beneficial to wives’ interests, and other forms of polygyny that favor the husband’s interests. See also Hamilton 1974 on the importance of a mutually supportive social group composed of matrilineally related females—mothers, when a woman is younger; daughters, when older.

  37. For estimates of degrees of relatedness among Mardu women, see Scelza and Bliege Bird 2008, Table 3. The average degree of relatedness among langurs w
as first estimated to be about 0.16 on the basis of behavioral observations (Seger 1977) and later confirmed when genetic evidence became available (Little et al. 2002).

  38. See Hamilton, Stoneking, and Excoffier 2005 for a particularly well documented example of more tightly regulated migration in patrilocal societies; see also Seilstad et al. 1998.

  39. Richards et al. 2003.

  40. Zerjal et al. 2003.

  41. See Hrdy 1999:249–265 and references reviewed therein; Knight and Power 2005.

  42. Reed et al. 2007. See Wade 2006 for an accessible and comprehensive overview.

  43. Wyckoff et al. 2000.

  44. Hrdy 1999:214–226. For fuller discussion, see Hrdy 1997, but that article was written before Alvarez and Hawkes convinced me to change my mind about hominin patrilocality.

  45. Paul et al. 1993 for Barbary macaques; Nicolson 1987 for olive baboons; Borries 1988 for langurs. Survey data for women who give birth after age 35 similarly suggest increased psychological commitment with age in a sample of contemporary American mothers (Gregory 2007).

  46. See Collins et al. 1984 for savanna baboons; Hrdy and Hrdy 1976 and Hrdy 1977a for langurs; Paul 2005 for captive sooty mangabeys and general overview.

  47. Collins et al. 1984:208 and Table 4.

  48. Seger 1977; Little et al. 2002.

  49. Fairbanks 1988.

  50. Pavelka, Fedigan, and Zohar 2002; Fairbanks and McGuire 1986; Fairbanks 2000; Hasegawa and Hiraiwa 1980; reviewed in Paul 2005. See Hrdy 1981a:110–111 for discussion of monkey mothers biasing support toward reproductively most “vulnerable” daughters. For parallels among human foragers, see Blurton Jones et al. 2005b; Kramer 2008.

  51. Fairbanks 1988, 1993; Paul 2005.

  52. Williams 1957; Hamilton 1966; first applied to primates by Hrdy and Hrdy 1976.

  53. For example, Pavelka 1990, cited in Paul 2005:22; see also Pavelka and Fedigan 1991.

  54. Silk et al. 2003.

  55. Paul 2005. For example, Fairbanks and McGuire 1986 for vervets; Pavelka et al. 2002 for Japanese macaques. Although I focus here on primate examples, the presence of the mother’s mother means larger litters, fewer losses, and so forth, in some other social mammals as well. Bushy-tailed wood rats (Neotoma cinerea) and wood mice (Apodemus sylvaticus) provide particularly well documented examples (Moses and Millar 1994; Gerlach and Bartmann 2002).