Comparative Biochemistry and Physiology Part A 136 (2003) 85–94 Review Testing evolutionary hypotheses about human biological adaptation using cross-cultural comparison૾ Ruth Mace*, Fiona Jordan, Clare Holden Department of Anthropology, University College London, Gower St, London WC1E 6BT, UK Received 4 July 2002; received in revised form 16 January 2003; accepted 17 January 2003 Abstract Physiological data from a range of human populations living in different environments can provide valuable information for testing evolutionary hypotheses about human adaptation. By taking into account the effects of population history, phylogenetic comparative methods can help us determine whether variation results from selection due to particular environmental variables. These selective forces could even be due to cultural traits—which means that gene- culture co-evolution may be occurring. In this paper, we outline two examples of the use of these approaches to test adaptive hypotheses that explain global variation in two physiological traits: the first is lactose digestion capacity in adults, and the second is population sex-ratio at birth. We show that lower than average sex ratio at birth is associated with high fertility, and argue that global variation in sex ratio at birth has evolved as a response to the high physiological costs of producing boys in high fertility populations. ᮊ 2003 Elsevier Science Inc. All rights reserved. Keywords: Comparative method; Human sex ratio; Lactose tolerance; Phylogeny; Gene-culture co-evolution; Adaptation; Maternal mortality; Natural selection 1. A phylogenetic approach to testing evolution- is occurring). However, a simple, statistical corre- ary hypotheses using cross-cultural data lation between traits across cultures is complicated by the non-independence of cultures, as was first Physiological data from a range of human pop- recognized in the 19th century by Francis Galton. ulations living in different environments can pro- The same problem applies in cross-species com- vide valuable information for testing evolutionary parisons. Evolutionary biologists have developed hypotheses about human adaptation. The compar- phylogenetic comparative methods that can take ative method can help us determine whether vari- account of the hierarchical inter-relatedness of ation results from selection due to environmental species and test for the co-evolution of traits on factors, or is possibly selected for by cultural phylogenetic trees. Mace and Pagel (1994) argued forces (which means that gene-culture co-evolution that similar approaches can be used to test cross- ૾ This paper is part of a collection of inter-disciplinary, cultural hypotheses. In this paper, we will outline peer-reviewed articles under the Theme: ‘‘Origin and Diversity two examples of the use of these approaches to of Human Physiological Adaptability’’ invited by K.H. test adaptive hypotheses explaining global varia- Myburgh and the late P.W. Hochachka. tion in two physiological traits: the first is lactose *Corresponding author. Tel.: q44-20-7679-2463; fax: q44- 20-7679-7728. digestion capacity in adults, and the second is E-mail address: [email protected] (R. Mace). population sex-ratio at birth. In the case of lactose 1095-6433/03/$ - see front matter ᮊ 2003 Elsevier Science Inc. All rights reserved. doi:10.1016/S1095-6433(03)00019-9 86 R. Mace et al. / Comparative Biochemistry and Physiology Part A 136 (2003) 85–94 Fig. 1. Two possible scenarios in which A9 is evolving with B9. (a) A case in which four populations showing A9B9 and five populations showing AB could represent only one independent instance of B evolving into B9 after A had evolved into A9. (b) A case in which four populations showing A9B9 represents four independent instances of A evolving in A9 followed by B evolving into B9. digestion capacity we review work we have pre- differ between Africa and Europe. A genetic trait viously published elsewhere. The study of sex co-evolving with sunshine, or malaria, or polygy- ratio variation is new. ny, to name some arbitrary examples, could equally Hierarchically related units, be they species or underlie the observed trend. Each population in populations, cannot be considered as statistically Africa differing from one in Europe does not independent in comparative tests. Below, we report represent an independent test of the hypothesis that sex ratio at birth is more male-biased in that nutrition is influencing sex ratio, because the European than in African countries. This could be populations in Africa are likely to be closely related to higher levels of malnutrition in Africa. related to each other, as are those in Europe. Fig. A simple statistical correlation across African and 1 illustrates how a similar correspondence between European populations with some correlate of nutri- two traits across related populations could repre- tion might yield a highly significant result. How- sent as little as one or as many as four independent ever, there are a large number of variables that cases of co-evolution. Clearly the latter (Fig. 1b) R. Mace et al. / Comparative Biochemistry and Physiology Part A 136 (2003) 85–94 87 provides stronger evidence for the traits co-evolv- equally related, which we know is wrong. Net- ing than the former (Fig. 1a). Evolutionary biolo- works would be very hard to estimate, and current gists have developed a number of statistical statistical procedures cannot test for correlated approaches in which evidence for a change along evolution using networks. In the tests reported the branches of a phylogenetic tree are linked to here, we do use phylogenetic trees of human independent instances of change in the relevant cultures based on genetic similarity (Cavalli-Sforza trait (Felsenstein, 1985; Harvey and Pagel, 1991; et al., 1994). The weight of anthropological, genet- Pagel, 1999). ic and archaeological knowledge indicates that, Mace and Pagel (1994) argued that similar almost whatever the degree of cultural isolation, approaches can be used to test cross-cultural com- some populations are much more closely related parative hypotheses in biological and cultural to some cultures than they are to others. So anthropology. Formal methods originating in evo- whatever the shortcomings of a phylogenetic mod- lutionary biology can be used to construct phylog- el of history, it is likely to be the best we have for enies of cultures. Models of human population our purposes here. Thus, whether the traits of history can be inferred using genetic or linguistic interest are predominantly genetically, environmen- data. These have been developed not only using tally or culturally determined, phylogenetic regres- allele frequencies to construct population genetic sions are appropriate. trees (e.g. Cavalli-Sforza et al., 1994) but also The statistical comparative methods we use in from the application of phylogenetic algorithms to the examples reported here are based on maximum cognate words in language groups (Gray and likelihood (Pagel, 1994, 1999). ML is used to test Jordan, 2000; Holden, 2002). Some debate has whether the rate of change in a trait on each arisen as to whether phylogenies, a descriptive branch of the phylogenetic tree is influenced by tool normally used to describe the evolutionary the other trait on that branch of the phylogenetic relationships between species, can actually be tree. A model of independent evolution is fit and applied within species. Attempts to classify human compared with a model in which the rate of change racial groups genetically have not found discrete in one trait is influenced by the presence or groups, but geographic clines of variation. Clearly absence of the other trait. If the dependent model some cross-cultural interbreeding occurs, such that is significantly more likely than the independent several anthropologists have argued that a network model, then this provides statistical evidence that might strictly represent population history better the two traits are co-evolving. This method can be than a phylogenetic tree (Bateman et al., 1990; applied to discrete traits, and a similar method can Bellwood, 2001; Moore, 1994). Trees based on be applied to continuous traits. In the case of language may actually suffer less from this prob- lactose digestion capacity, the frequency distribu- lem of mixing, as immigrants into new communi- tion of levels of lactase persistence in native ties tend to leave behind or at least fail to pass on populations is bimodal; most un-mixed populations their native language, whereas they bring their show either very high or low levels of lactase genes with them and do pass them into future persistence with a trough of populations with generations. Hence it is possible that language approximately 70% of individuals showing lactose trees are more tree-like than human population tolerance (Holden and Mace, 1997, 2002). Hence genetic trees. Using shared cognate words to gen- we use the method DISCRETE for discrete char- erate trees of human cultures does produce trees acters (Pagel, 1994, http:yywww.ams.rdg.ac.uky that resemble historical patterns inferred from zoologyypagely). Variation in sex-ratio at birth is either archeological or historical sources. Both a continuous trait, so in that case we used the Gray and Jordan (2000) analyzing Pacific lan- CONTINUOUS method, which is based on gen- guages, and Holden (2002) analyzing Bantu lan- eralized least squares (GLS) phylogenetic regres- guages, found that evolutionary relationships sion (Pagel, 1997, 1999, http:yywww.ams.rdg. between languages suggested historical migration ac.ukyzoologyypagely). patterns similar to those proposed by archae- 2. The evolution of lactose tolerance as an ologists. adaptation to pastoralism Any statistical comparison does require some explicit model of evolutionary history; not using a Fig. 2 shows the distribution of the frequency tree is equivalent to assuming all cultures are of high, moderate or low ability to digest lactose 88 R. Mace et al. / Comparative Biochemistry and Physiology Part A 136 (2003) 85–94 Fig. 2. Variation in levels of lactose tolerance in 56 populations where it has been measured.