Original reference:
Moore, J. (1992). Sociobiology and incest avoidance: a critical look at a critical review. Amer. Anthropol. 94: 930-933.
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Sociobiology and incest avoidance:
A critical look at a critical review

Jim Moore
Anthropology Dept.
University of California, San Diego
La Jolla CA 92093
jjmoore@ucsd.edu

I sympathize with Gregory C. Leavitt's stated goal in critiquing the evidence upon which early sociobiological analyses of human incest avoidance are based (A. A. 92: 971-993, 1990). In fact, Rauf Ali and I wrote an analogous critique of the data used to support the inbreeding-avoidance hypothesis for sex-biased dispersal among animals (Moore & Ali, 1984), which he cites favorably. Unfortunately, Leavitt goes on to evaluate sociobiological theories themselves (e.g., p. 984). The distinction is important because most of the articles he criticizes were written between 1975 and 1983. Thus Leavitt's stated goal is not his actual destination, and his rejection of a sociobiological theory is accomplished without considering most of the relevant biological and ethological literature of the last decade.

A second problem is that there are a number of missleading statements in the presentation of material he does consider. If all anthropologists read widely in these fields, the paper would be read for its good points, these errors quietly forgotten. This is not the case; how many American Anthropologist readers are familiar with Baker's work on white-crowned sparrows, which Leavitt (mis-)cites? Since incest avoidance is one of anthropology's central problems, a comment on some of those errors seems worthwhile.

Cultural universals:

Leavitt states that sociobiologists have dealt with "noncompliance" with incest taboos by "redefining incest." Both social and biological sciences use the terms "inbreeding" and "incest," often imprecisely, and this does lead to confusion as is clearly illustrated throughout Leavitt's article by his failure to distinguish inbreeding from incest (e.g., p. 975 discussion of "outbreeding mechanisms posited by human sociobiology" (avoiding incest [is not equal to] outbreeding)). (See Shields (1987) and Thornhill (1991) for discussion of definitional issues.)

Earlier in his article, Leavitt states that:
The argument that environmental factors can produce exceptional cases ... only further complicates the specification discussed above; for example, what is unusual in the Roman, Egyptian, Arapesh, or Mormon environments that nullifies the genetic imperative hypothesized? The hypothetical interjection of environmental variables also produces a set of theoretical problems that natural selection theory seems as yet ill-equipped to handle... (pp. 973-4, emphasis added).

By analogy he presumably would argue that the existence of a secular trend in adult height demonstrates the absence of any genetic influence on stature. (For discussion of the sociobiological "problem" of environmentally-correlated variation in behavior, see Wilson (1975), Krebs & Davies (1987), Hrdy (1990), or any issue of Behavioral Ecology and Sociobiology.) Space precludes full discussion of factors that can promote incestuous behavior. Two are (1) sexual asymmetry in parental investment, leading to the prediction that the "less-investing sex" (males in most mammals) should be relatively more tolerant of incest; and (2) the distribution of resources important to members of a relatively K-selected species, such that inbreeding may result from territory retention or resource monopolization within a kin group (cf. "royal incest" in humans) (see, e.g., Smith, 1979; Moore & Ali, 1984; Thornhill, 1991).

Inbreeding effects:

According to Leavitt, among Pleistocene hominids genetic loads would have been low but "any system of inbreeding that is reasonably possible would not greatly reduce the heterozygosity of the population" (p. 975). However, genetic load is reduced by the cumulative "weeding" effect of exposure of lethal recessives in homozygotes. Unreduced levels of heterozygosity and genetic loads approaching zero are simply incompatible. Even one or two transfers between social groups per generation would prevent the elimination of genetic load he postulates; such groups are socially "isolated" and they would probably be somewhat inbred, but one cannot conclude from this that nuclear family incest would not result in inbreeding depression. (See Ralls, Harvey and Lyles (1986: 52-54) for a lucid discussion.)

Ethological studies:

The distinction between cited early evidence and current theory is vital here; claims of virtually complete endogamy among baboon and macaque groups reported during the 1960s have been rejected for more than a decade, a fact Leavitt fails to mention (for review see Pusey & Packer, 1987). There are also problems with the representation of articles he does discuss.

Leavitt implies that Erickson (1989) was misleading in his treatment of Itoigawa, Negayama and Kondo (1981), and emphasizes that Itoigawa et al. reported mother-son copulation in Japanese macaques. However, the methods employed by Itoigawa et al. were explicitly designed to promote mother-son copulation; even so, incestuous copulations were rare and behaviorally atypical. Under severe sociosexual deprivation, sexual disinterest (including incest avoidance) apparently can be overcome. Leavitt asked for examples of "the environmental factors that produce incestuous behavior" (p. 974); here is one.

Erickson's handling of Sugiyama & Koman's work on chimpanzees is also criticized: "What Erickson fails to report is that Sugiyama & Koman ... also observed ten cases of mother-son copulation" (Leavitt, p. 979). Leavitt fails to report that all ten cases involved two infant males (Sugiyama and Koman, 1979). This hardly sounds like sexual aversion, but mother-son nonreproductive sexual behavior is still consistent with a sociobiological framework. If nonhuman primates can be allowed psyches, the psychological aspects of such behavior should prove a fascinating area for study.

Most troubling in his review of primate literature is his failure to mention Pusey's work on chimpanzees (Pusey, 1980), which was discussed by all of Leavitt's "target authors" writing post-1980. Furthermore, in our data review (cited by Leavitt), Ali and I explicitly state that "chimpanzees fit the inbreeding-avoidance model [for dispersal] precisely" in part because among chimpanzees "behavioral incest avoidance is well developed ..." (1984:104), as shown by Pusey's presentation of clear evidence for the behavioral avoidance of sibling, mother-son, and (potential) father- daughter incest. More recently, Goodall describes the few cases of mother-adult son copulation observed at Gombe National Park: in two of three such interactions in which intromission was observed, the "mother protested violently, screamed, [and] pulled away prior to ejaculation" (Goodall, 1986:466-467).

Leavitt concludes his summary of the ethological data with a list of 16 studies "...(largely ignored by human sociobiology) that report close inbreeding" (p. 980, emphasis added). Here is what one of them, an analysis of the genetic consequences of song dialect recognition in sparrows, really says:

The relationship among the calculated F-statistics [measures of inbreeding] is that the total inbreeding coefficient of an average individual within a dialect (FIT) is primarily a result of the population being subdivided into relatively isolated dialects (FST) and is not at all due to consanguineous mating patterns within the dialect (FIS). In fact, the average FIS is negative which indicates that close inbreeding is actually avoided. (Baker, 1982: 567, emphasis added).

In others of the 16, close inbreeding is merely inferred (e.g. R. Smith, 1979) or is clearly due to lack of choice (wolves isolated on Isle Royale cited by Livingstone, 1980; captive rhesus macaques in a pen; D. Smith, 1982). Lack of options for an island-bound group is certainly an environmental factor, and behavioral mechanisms for incest avoidance are not expected to be strong in animals which (for demographic reasons) rarely encounter opportunities for incest (Moore & Ali, 1984).

Many studies (some of which appear in Leavitt's list) have found evidence of inbreeding in animal populations, and these have lead to the concept of optimal inbreeding (Shields; 1982) or optimal outbreeding (Bateson; 1983). Bateson's discussion should be of interest to anthropologists: he demonstrates a mating preference for unfamiliar first cousins among Japanese quail and argues on biological grounds that cousins might be preferred mates in other taxa as well (see Hoogland, 1992, and Moore, 1993, for recent review and data).

The field of human sociobiology certainly has its problems (see commentaries following Thornhill, 1991) but Leavitt's article does little to help solve them.

Notes

Acknowledgements. I thank Jack Bradbury, Nancy Friedlander, Owen Lovejoy, Mel Spiro, and Robert Tompkins for their comments.

References Cited

Baker, Myron C. 1982 Vocal dialect recognition and population genetic consequences. American Zoologist 22: 561-570.

Bateson, Patrick 1983 Optimal outbreeding. In Mate Choice. Patrick Bateson, ed. Pp. 257-277. Cambridge: Cambridge University Press.

Erickson, Mark 1989 Incest avoidance and familial bonding. Journal of Anthropological Research 45: 267-291.

Goodall, Jane 1986 The Chimpanzees of Gombe: Patterns of Behavior. Cambridge: Harvard University Press.

Hoogland, John L. 1992 Levels of inbreeding among prairie dogs. American Naturalist 139: 591-602.

Hrdy, Sarah Blaffer 1990 Sex bias in nature and history: A late 1980s reexamination of the "biological origins" argument. Yearbook of Physical Anthropology 33: 25-37.

Itoigawa, N., K. Negayama, and K. Kondo 1981 Experimental study on sexual behavior between mother and son in Japanese monkeys (Macaca fuscata). Primates 22: 494-502.

Krebs, John R. and Nicholas B. Davies 1987 An Introduction to Behavioural Ecology. Sunderland (MA): Sinauer.

Livingstone, Frank B. 1980 Cultural causes of genetic change. In Sociobiology: Beyond Nature/Nurture? George W. Barlow and James Silverberg, eds. Pp. 307-329. Boulder (CO): Westview Press.

Moore, Jim 1993 Inbreeding and outbreeding in primates: What's wrong with "the dispersing sex"? In The Natural History of Inbreeding and Outbreeding: Theoretical and Empirical Perspectives. Nancy W. Thornhill, ed. Chicago: University of Chicago Press. (in press)

Moore, Jim and Rauf Ali 1984 Are dispersal and inbreeding avoidance related? Animal Behaviour 32: 94-112.

Pusey, Anne E. 1980 Inbreeding avoidance in chimpanzees. Animal Behaviour 28: 543-582.

Pusey, Anne E. and Craig Packer 1987 Dispersal and philopatry. IN Primate Societies. Barbara B. Smuts, Dorothy L. Cheney, Robert M. Seyfarth, Thomas T. Struhsaker, and Richard W. Wrangham, eds. Pp. 250-266. Chicago: University of Chicago Press.

Ralls, Katherine, Paul H. Harvey and Anna Marie Lyles 1986 Inbreeding in natural populations of birds and mammals. In Conservation Biology: The Science of Scarcity and Diversity. Michael E. Soule, ed. Pp. 35-56. Sunderland (MA): Sinauer Assoc.

Shields, William M. 1982 Philopatry, Inbreeding, and the Evolution of Sex. Albany: SUNY Press.

Shields, William M. 1987 Dispersal and mating systems: Investigating their causal connections. In Mammalian Dispersal Patterns. B. Diane Chepko-Sade and Zuleyma Tang Halpin, eds. Pp. 3-24. Chicago: University of Chicago Press.

Smith, R. H. 1979 On selection for inbreeding in polygynous animals. Heredity 43: 205-211.

Smith, David G. 1982 Inbreeding in three captive groups of rhesus monkeys. American Journal of Physical Anthropology 58: 447-451.

Sugiyama, Yukimaru and Jeremy Koman 1979 Social structure and dynamics of wild chimpanzees at Bossou, Guinea. Primates 20: 323-339.

Thornhill, Nancy W. 1991 An evolutionary analysis of rules regulating human inbreeding and marriage. Behavioral and Brain Sciences 14: 247-293.

Wilson, Edward O. 1975 Sociobiology: The New Synthesis. Harvard: Harvard University Press.