Testing life history theory in a contemporary African population Meij, J.J.

Hele tekst

(1)Testing life history theory in a contemporary African population Meij, J.J.. Citation Meij, J. J. (2008, February 21). Testing life history theory in a contemporary African population. Retrieved from https://hdl.handle.net/1887/12615 Version:. Corrected Publisher’s Version. License:. Licence agreement concerning inclusion of doctoral thesis in the Institutional Repository of the University of Leiden. Downloaded from:. https://hdl.handle.net/1887/12615. Note: To cite this publication please use the final published version (if applicable)..

(2) 86.

(3) Chapter 5 Quantity trades off with quality of human offspring unexplained. by. differences. conditions. submitted. JJ Meij D van Bodegom JB Ziem J Amankwa AM Polderman TBL Kirkwood AJM de Craen RGJ Westendorp. 87. in. environmental.

(4) Summary Fitness of a species is determined by the ability of an organism to pass its genes. to. the. next. generations. under. defined. environmental. conditions.. Fitness is therefore dependent on fertility per se, and maintenance, in order to survive up to reproductive age. Life history theory predicts that limited resources are divided among these traits, resulting in a trade-off between investments. in. fertility. and. investments. in. maintenance.. Under. adverse. environmental conditions, resembling the habitat of our recent evolutionary past, we tested whether number and early survival of human offspring is inversely correlated. We studied 2460 women aged 25 years and over in an area in North East Ghana where both fertility and mortality levels are high. Proportional. survival. of. offspring. decreased. 4.0. %. (p<0.001). for. each. additional delivery, reducing from more than 90% among mothers who had less than four deliveries to about 50% among mothers who had more than twelve deliveries. As the association between number and early survival of offspring is often confounded by socio-economic status, in this population with a polygamous family structure, we also compared pairs of co-wives in 297 compounds who share identical environmental conditions. Offspring survival. decreased. 2.2. %. (p=0.012). for. each. additional. delivery. of. the. mother. When all 2460 women were analysed in a multivariable model controlling for differences in age, environment, and tribal structure, each additional delivery of the mother resulted in a 2.4 % (p<0.001) lower proportional survival of their offspring. We conclude that the inverse correlation between. quantity. and. quality. of. offspring. is. independent. of. local. environmental conditions. This provides evidence for a genetically encoded trade-off between investments in fertility and maintenance in humans.. 88.

(5) Introduction Fitness of a species is determined by the ability of an organism to pass its genes. to. the. next. generations. under. defined. environmental. conditions.. Fitness is therefore dependent on both fertility per se, i.e. the number of offspring,. and. maintenance,. i.e.. the. survival. of. this. offspring. up. to. reproductive age. Life history theory predicts that natural selection optimizes the life history traits of organisms to best fit the prevailing environmental conditions.. Limited. resources. are. divided. among. key. life. history. traits,. resulting in a trade-off between quantity and quality of offspring (Ross 1992; Stearns. 1992).. As. a. result. of. natural. selection,. species. differ. in. their. combinations of life history traits, often referred to as life history strategies. The. comparison. of. different. animal. species. shows. a. strong. negative. association between number of offspring and both parental and offspring survival, which is in line with the predicted trade-off between fertility and maintenance.. The trade-off between investments in fertility and maintenance is also present within one species. First evidence for this notion was found from artificial selection experiments in the fruit fly Drosophila melanogaster (reviewed in Rose et al. 2002; Sgro et al. 2000). A selection regime favoring flies with prolonged fertility at later ages resulted in populations with reduced fertility early in life and increased life span. Direct selection for longevity produced long-lived populations with a significantly reduced fertility (Zwaan et al. 1995). Studies on the nematode Caenorhabditis elegans also showed that mutations in the insulin pathway are associated with an increase in life span at the cost of fertility (Arantes-Oliveira et al. 2002; Arantes-Oliveira et al. 2003). Taken together, these experiments underpin a genetically encoded, biomolecular mechanism for the tradeoff between fertility and maintenance.. Next to experimental organisms, observational studies on birds have shown that. increased. reproductive. effort. is. associated. with. increased. parental. mortality (Daan et al. 1996). Moreover, there is accumulating evidence that the. trade-off. between. fertility. and. maintenance. may. also. be. present. in. humans. Earlier, we have studied a historic data set of the British aristocracy and found that the total number of offspring, an estimate of fertility, was negatively. correlated. maintenance. with. (Westendorp. longevity, &. an. Kirkwood. estimate 1998).. of. investments. Several. studies. in. have. confirmed these findings (Doblhammer & Oeppen 2003; Korpelainen 2000; Smith et al. 2002; Thomas F. et al. 2000). A study in Gambia did not find an association between number of offspring and female mortality (Sear 2007). A recent review of the association between number of offspring and female mortality shows the predicted association in most historic studies under. 89.

(6) adverse. conditions. whereas. it. is. absent. in. contemporary. studies. under. affluent conditions (Hurt et al. 2006). Most studies have concentrated on the trade-off within one generation, studying the trade-off between investments in reproduction and investments in survival of the same individual. However, an observational study on the trade-off between female fertility and early survival of offspring could provide evidence that these life history traits have a genetic basis and can therefore be transposed also to the next generations, as is predicted from the selection experiments.. Several studies have already investigated trade-offs between number and early. survival. of. offspring. in. contemporary. human. populations.. Studies. among 491 women of the !Kung of Botswana (Pennington & Harpending 1988) and among 324 women of the Ache of Paraquai (Hill & Hurtado 1996) found a positive and linear association between number and early survival of offspring without showing a plateau at higher numbers of offspring. A study among 167 women of the Dogon of Mali showed a positive non-linear association between number and early survival of offspring (Strassmann & Gillespie 2002). The clear absence in these studies of a negative association between number and early survival of offspring, however, could well be explained by confounding by socio-economic status, i.e. women with higher status have larger families that experience lower mortality because of better environmental conditions (Borgerhoff Mulder 2000). Therefore, we have set up a large cohort to study maternal fertility patterns and offspring survival among 2460 women under environmental conditions in northern Ghana, resembling the human recent evolutionary past. Because the people in the study have a polygamous family structure, we had the unique opportunity to adjust for differences in socio-economic status by comparing number of offspring and early survival in pairs of co-wives from the same compound, thus sharing the same socio-economic environment.. Methods Research area The study was conducted in the remote Garu-Tempane district in the Upper East region of Ghana, a densely populated agricultural area. In 2001, the research area was explored by the Department of Parasitology of the Leiden University. Medical. Centre. which. set. up. a. database. for. parasitological. research (Ziem et al. 2005). In this database name, sex, estimated age, tribe, and location of the compound were registered. We started our study by using this database and added detailed demographic information about fertility and child mortality.. The Garu-Tempane district is inhabited by several tribes; mostly Bimoba. 90.

(7) (66%) and Kusasi (24%). Compared with the south of Ghana, the whole of the. Upper. East. region,. and. especially. the. Garu-Tempane. district,. is. underdeveloped. The estimated gross domestic product per capita is less than $ 100 in this region, while the gross domestic product per capita for the whole of Ghana is $ 2050. The region has a semi-Saharan climate with an average temperature of 32 ºC throughout the year with one annual rain season from June to August. The research area around the village of Garu measures. 2 2 approximately 375 km with an estimated density of 66 inhabitants per km .. Most of the people are farmers and the agricultural process is entirely done by manual labour. Recently, some health clinics have been set up in the area, but these are not fully in service yet. Hospitals and other medical services are absent. Vaccination of children was introduced in the early 1990s. In 2003, about 50% of the children under 10 years had been vaccinated at least once for either measles, polio or diphtheria.. As estimated from our 2003 and 2004 surveys, migration is very low and amounts to less than 1% per year. Most migrants are young men who move to the larger cities in Ghana to work in seasonal occupations. All individuals live in extended family compounds. Each compound consists of a number of separate huts linked by a surrounding wall (see map of Bimoba compound on page38). The oldest man in the compound is head of the family (land lord) and generally takes care of up to four wives. Within the compound the individual women have their own hut but activities such as farming and child care are a shared responsibility. Although food preparation and cleaning are private activities, food at the compound is shared during communal meals. All children share the same hut and the custom of formula-feeding infants is absent.. In the study area, most women begin sexual activity around the age of fourteen and most give birth before the age of eightteen. Birth control is virtually. absent,. although. spacing. of. children. by. means. of. prolonged. breastfeeding is sometimes practised by younger women. Most women want to have as many children as possible, since large family sizes are highly regarded.. Subjects and methods All. villages. and. compounds. were. mapped. with. the. Global. Positioning. System in 2001 and 2002. Since there are no civil registries, all villages and compounds within the study area were registered and assigned an unique identification number. The name, sex, age, and tribe of each individual was registered.. In. total. 24,801. individuals. were. registered. in. the. original. database, living in 2,350 compounds, including 4,016 women aged 25 years. 91.

(8) and over.. In 2003 we revisited all compounds in the research area. During these field visits the database was updated and all women of 25 years and older who were present at their compound (n = 2,479) were invited to participate in the present. survey.. As. most. women. are. illiterate,. witnessed. oral. informed. consent was obtained by a local translator. Nineteen women refused cooperation. Both the Ethical Review Committee of the Ghana Health Service and the Medical Ethical Committee of the Leiden University Medical Centre in Leiden, The Netherlands, approved this study.. Demographic characteristics Age. of. women. was. estimated. as. the. average. from. three. independent. observations by local and Dutch researchers in 2003. Data on the number and survival. status. of. all. births. were. retrieved. in. line. with. the. Ghana. Demographic and Health Surveys (DHS), an internationally representative household survey for monitoring and impact evaluation of indicators in the areas of population, health, and nutrition (Ghana Statistical Service 2004; Sorensen et al. 1988). To obtain the most accurate information, we set up compound interviews under supervision of local co-workers, assisted by translators,. in. which. all. women. who. were. present. in. the. compound. participated. During these interviews the women discussed with each other the number of deliveries they had had, including the number of children who had died and the number of children who were still alive. These interviews increased. the. encounter. any. accuracy. of. hesitation. to. the. information. openly. discuss. considerably these. as. matters.. we. Based. did. not. on. the. number of deliveries and the number of children still alive, we calculated the proportional survival of the offspring for each mother as the number of surviving children divided by the number of deliveries.. Village interviews To obtain information on reproduction strategies of women we set up a series of. village. interviews.. Five. groups. of. twenty. women,. all. coming. from. different villages, were interviewed by two female co-workers. During these interviews information was obtained about the desired number of offspring, reproduction, spacing strategies, and use of contraceptives.. Statistical analysis All. outcome. parameters. are. presented. as. means. with. standard. errors.. Proportional survival over strata of maternal fertility were compared by linear regression analysis. Because the observations on proportional survival may not have been evenly distributed in strata with smaller numbers, we. 92.

(9) performed. an. additional. non-parametric. analysis. using. the. Jonckheere-. Terpstra test for trend.. To exclude possible distortion of the relation between maternal fertility and proportional survival of their offspring by local environmental and socioeconomic differences, we compared women within each compound. To do this, we selected compounds in which we identified pairs of co-wives within an ageband of ten years. We then regressed the difference in proportional survival of their offspring on the difference in number of deliveries between the co-wives. As a check on the possible confounding effect of age, we repeated the compound analysis with a restriction to co-wives within an ageband of five years.. Since proportional survival was assessed at a single time point (the time of the study), and therefore might have been influenced by the ages of the different children, we also studied the association among women aged 45 years. and. over,. as. they. are. post-menopausal. for. 5. years. or. longer. We. estimated the menopausal age in this area to be around 40 years. By selecting this group we excluded pre-menopausal bias as well as the bias of young children still at risk. In this way we defined offspring survival as survival up to age 5, since child mortality beyond this age is low (Borgerhoff Mulder 1988).. Finally,. we. analyzed. the. association. between. number. of. offspring. and. proportional offspring survival in all women using linear mixed models with compound as a random factor and age of women and tribe as covariates. All calculations were performed with SPSS version 12.0.. Results Table. 1. women. (next who. page). were. shows. included. the in. demographic our. study. We. characteristics found. 18. of. (0.7. the. %). 2460. women. reporting to have had no deliveries, whereas seven women (0.3%) reported having had fifteen deliveries. The distribution of the number of deliveries in Bimoba. women. was. similar. to. the. distribution. in. the. whole. population. indicating that the maternal fertility pattern between tribes is not different. Mean number of deliveries was 6.3 (SE 0.05) for all women and 7.7 (SE 0.07) for women aged 45 years and over.. Table 2 (page 95) shows the relationship between number of deliveries and propor-tional survival of the offspring for the 2442 women with at least one delivery. Among these women there was a highly significant, progressive decrease in proportional survival with increasing family size.. 93.

(10)

(11)

(12)

(13) Table 1. Demographic and Fertility characteristics of the 2460 women included in rthe study.. . .

(14)

(15) . .

(16) .

(17)

(18) !. . . ". #$ . !. !. . . # . #. ". #. $. # . $. ". . $. #" . !#. . ". ##. . #". . . ##. ## . ". ". !. #!. " . ". ". . "#. ! . "". !. $. #. "# . !". $!. . ". " . . !#. . ". "!! . . !. . . # . . . #. . "$"! . #. $!. . #. "# . !. !. ". !. $ . . !. . %

(19) " & ' . We. calculated. proportional. a. 4.0%. offspring. (95%CI. survival. 3.7%. for. –. each. 4.3%,. p<0.001). additional. decrease. delivery.. A. in. similar. decrease of 4.1% (95%CI 3.7% – 4.5%, p<0.001) per additional delivery was observed when we analysed only the women of the dominant Bimoba tribe. in proportional survival for each additional delivery was 2.8% (95%CI 2.2%. In our analysis of the subgroup of post-menopausal women only, the decrease – 3.4%, p<0.001) for all postmenopausal women and 2.8% (95%CI 2.1 – 3.6, p<0.001). for. the. postmenopausal. Bimoba. women. only.. possiblity that the significance level was due to a skewed. To. exclude. the. distribution of. observations, especially because the observations in the extremely low and extremely high delivery groups are limited, we performed an additional nonparametric analysis. The negative association between number of deliveries of the mother and proportional offspring survival remained highly significant for all comparisons (Jonckheere-Terpstra test, all p<0.001).. 94.

(20)

(21)

(22)

(23)

(24) Table 2. Proportional offspring survival dependent on the number of deliveries of the. . mother.. . .

(25)

(26) . . . !

(27) . !

(28) " . . . !. ". ". . ". . " . . !. ". . "!. . . ". . ". . . ". !. . . . !. . . . . ". . . . ". . . . . . . . . ". ". . . . . . . !. . . ! !. !". !. . !. !. !. ! . !. ". ! . ! . ! . . !. !. . . #

(29) . $

(30) % $ !& '(

(31) )

(32) . To. exclude. the. environmental. possibility. conditions. that. as. a. our. findings. result. of. could. be. accounted. socio-economic. for. differences,. by we. performed an analysis among co-wives within compounds. We selected 297 Bimoba compounds with pairs of co-wives of similar age, defined as a maximum age difference of ten years. We then regressed the difference in proportional offspring survival on the difference in number of deliveries between the co-wives. Within pairs of co-wives of the same compound, proportional offspring survival was significantly lower among women with more deliveries (figure 1). Survival of children decreased 2.2 % (95%CI 0.5% – 3.9%, p=0.012, Jonckheere-Terpstra p=0.006) for each additional delivery of the mother. When we further restricted the analysis to a maximum age difference of five years (N=229), we observed a 2.3% (95%CI 0.3% – 4.4%,. p=0.023,. Jonckheere-Terpstra,. p=0.017). decrease. in. offspring survival for each additional delivery of the mother.. 95. proportional.

(33) Figure 1. Differences in proportional offspring survival dependent on the difference in. number. of. deliveries. in. 297. pairs. of. Bimoba. co-wives. who. live. in. the. same. compound. Data are presented as means and standard errors (p for trend = 0.012).. Finally, in the whole data set, we modelled the proportional survival of the children, dependent on the number of deliveries among co-wives within each compound, adjusting for age of the mother and tribe. Again, we found a highly. significant. negative. association. between. number. of. deliveries. of. mother and proportional offspring survival. For each additional delivery of the mother the offspring survival was 2.4 % lower (95%CI 2.0 –2.8, linear mixed model, p<0.001).. To analyse the association between the total number of offspring and the surviving number of children alive we compared the number of surviving offspring with the number of deliveries of the mother (figure 2, next page).. 96.

(34) Figure 2. Number of children alive among 704 post-menopausal Bimoba women with different fertility histories. Data are presented as means and standard errors.. In women aged 45 and over, there was a steady increase in the number of surviving offspring for the first nine deliveries. This steady increase levelled off in the delivery groups with 10 to 15 deliveries. Moreover, the mean number of surviving children did not exceed six for any number of deliveries.. 97.

(35) Discussion In a contemporary human population living under adverse environmental conditions with high fertility and mortality levels in North East Ghana, we found a highly significant decrease in proportional survival of offspring with increasing numbers of offspring. Since pressure on scarce resources might explain why mothers with larger numbers of children experienced lower offspring survival, we have also compared data for pairs of co-wives within polygamous families, who live in extended compounds in which they share resources and experience identical environmental conditions. This analysis showed. that. the. negative. association. between. number. of. offspring. and. offspring survival was similar to that seen across the study group as a whole. This pattern was unaffected when we selected only women of the principal tribal group (Bimoba) or when we considered postmenopausal women only. We conclude that our data show evidence for a strong negative association between number and survival of offspring that has, in part, a genetic basis. Several alternative explanations for the outcomes of our study need to be considered. First, the observed association between the number and survival of offspring might better be explained by differences in social position within the compound. An observation of this kind was made among the Kipsigis in Kenya, where women with more inherited land had higher esteem and better offspring survival (Borgerhoff Mulder 2000). Also in our research area, large families are regarded as a marker of esteem. As the wife with the highest social status would be expected not only to have more children but also to have better living conditions, it can thus be expected that their numerous offspring. would. have. opposite:. within. large. a. higher. proportional. families. survival. of. survival. offspring. We was. observed lowest.. It. the is. therefore unlikely that our observed association is caused by differences in social status. Second, another possible distorting variable was identified by a study on polygyny among the Dogon. Here, child mortality in polygynous households was higher than in monogamous households (Strassmann 1997). Since we found no change of effect when comparing pairs of co-wives living in polygynous compounds, this difference can not account for the observed association. Third, early mortality, especially neonatal mortality, is far less likely. among. breast-fed. infants. when. compared. to. formula-fed. infants. (WHO 2000; Wilson et al. 2006). As the habit of formula-feeding in our research area is virtually absent, this is unlikely to have influenced our results.. Fourth,. our. results. might. have. been. biased. because. of. vertical. transmission of the HIV virus. However, the sero-prevelance of HIV in the region. of. the. Demographic. research and. area. Health. is. very. Survey,. low. According the. to. the. 2003. Ghana. sero-prevalence. of. HIV. among. pregnant women in the whole region is 0.8% and among sexually active men. 98.

(36) it is 2.2% (Ghana Statistical Service 2004; Wilson et al. 2006). It is therefore unlikely that mother to child transmission of the HIV virus can explain our results. Finally, the higher proportional offspring survival among women who had a smaller number of deliveries could be the result of survival-based family planning. The reasoning being that a mother decides to have an extra delivery when one of her children has died . While this is a phenomenon seen in other societies, (Kimani M. 2001; Wilson et al. 2006) we do not think that this. explains. for. the. findings. presented. here.. All. interviewed. women. expressed the wish to have as many children as possible, independent of the individual survival of the children, therefore the effect of survival-based family planning is likely to be limited.. The fertility data of this large, homogeneous cohort of women show peculiar characteristics. We observed that the actual number of surviving children, unlike the proportional survival, levelled off among women with more than nine. children.. We. observed. a. maximum. mean. survival. of. six. children,. regardless of the number of deliveries. This indicates that the environmental conditions in combination with the biological make up of the women, limits the actual number of surviving children to six. Also, when compared to data from. affluent. societies,. the. distribution. of. the. number. of. deliveries. is. remarkable. First, the number of women with no deliveries is just 0.7%. This is very low compared to affluent societies where it is around 10 % (Evers 2002). Moreover, the percentage of women with one or two children is also low, which indicates that these women make only a marginal contribution to the next generation. Second, there were no women with more than fifteen deliveries. In affluent societies, the percentage of women with more than fifteen children is also low, but do exist. This suggests that under adverse environments the investments in body maintenance curtail the maximum number of offspring to fifteen.. All together, our data show a strong negative association between number and early survival of offspring. This is in line with findings from both experimental models and findings in human historic data. All arguments point out that. life. history. theory. can. also. be. applied. to. humans. and. that. natural. selection results in a trade-off between investments in fertility and maintenance. This explains for the strong negative correlation between quantity and quality of offspring that we have observed. Despite the general validity of the theory, the biological mechanism that accounts for this trade-off has yet to be elucidated. Earlier, we have proposed a plausible mechanism for this trade-off in humans (Westendorp et al. 2001). We hypothesize that the innate immune system is a critical factor driving an individual into the direction of either a high fertility or to a better maintenance strategy. As over. 99.

(37) thousands of years human survival has been highly dependent on resistance to. infectious. diseases,. genetic. adaptations. resulting. in. inflammatory. responses were favored. An inflammatory host response is critical to fight infection necessary to survive up to reproductive age. An inflammatory host response is also negatively associated with fertility because immunotolerance for the paternal antigens of the fetus is required for pregnancy to proceed succesfully. We have found preliminary evidence that specific inflammatory signaling cytokines are associated with survival to infectious diseases (van Dissel et al. 1998; Westendorp et al. 1997). These are the same cytokines that are negatively associated with fertility (Hill 1995; Makhseed et al. 2001; Westendorp et al. 2001).. Conflict of interest statement We have no conflict of interest.. Acknowledgements We thank Laar Baya Daniel, Konlan Nijagben Moses, Marleen van der Vorm, Yasha van den Berg, Diana Plug and Kombat Bakpen John for assisting in the fieldwork and prof Dr. J.P. Vandenbroucke for his helpful comments.. 100.

(38) 101.

(39) References. Arantes-Oliveira, N., Apfeld, J., Dillin, A. & Kenyon, C. 2002 Regulation of life-span by germ-line stem cells in Caenorhabditis elegans. Science 295, 502-505. Arantes-Oliveira, N., Berman, J. R. & Kenyon, C. 2003 Healthy animals with extreme longevity. Science 302, 611. Borgerhoff Mulder, M. 1988 The relevance of polygyny treshold model to humans. Cambridge University Press. Borgerhoff. Mulder,. M.. 2000. Optimizing. offsprings:. the. quantity-quality. tradeoff in agropastoral Kipsigis. Evolutionary Human Behaviour 21, 391410. Daan,. S.,. Deerenberg,. C.. &. Dijkstra,. C.. 1996. Increased. daily. work. precipitates natural death in the kestrel. Journal of animal ecology 65, 539544. Doblhammer, G. & Oeppen, J. 2003 Reproduction and longevity among the British peerage: the effect of frailty and health selection. Proc.Biol.Sci. 270, 1541-1547. Evers, J. L. 2002 Female subfertility. Lancet 360, 151-159. Ghana Statistical Service 2004 Ghana Demographic and Health Survey 2003. Calverton,. Maryland:. Noguchi. Memorial. Institute. for. Medical. Research. (NMIMR) and ORC Macro. Hill, J. A. 1995 T-helper 1-type immunity to trophoblast: evidence for a new immunological mechanism for recurrent abortion in women. Hum.Reprod. 10 Suppl 2, 114-120. Hill, K. & Hurtado, M. 1996 Ache life history: the ecology and demography of a foraging people.. New York: Aldine de Gruyter.. Hurt, L. S., Ronsmans, C. & Thomas, S. L. 2006 The effect of number of births on women’s mortality: systematic review of the evidence for women who have completed their childbearing. Popul.Stud.(Camb.) 60, 55-71. Kimani M. 2001 Behavioral effects of infant and child mortality on fertility in Kenya. 2001;5:63-72. Afr J Reprod Health 5, 63-72. Korpelainen, H. 2000 Fitness, reproduction and longevity among European. 102.

(40) aristocratic and rural Finnish families in the 1700s and 1800s. Proc.Biol.Sci. 267, 1765-1770. Makhseed, M., Raghupathy, R., Azizieh, F., Omu, A., Al Shamali, E. & Ashkanani, L. 2001 Th1 and Th2 cytokine profiles in recurrent aborters with successful pregnancy and with subsequent abortions. Hum.Reprod. 16, 22192226. Pennington, R. & Harpending, H. 1988 Fitness and fertility among Kalahari !Kung. Am.J.Phys.Anthropol. 77, 303-319. Rose, M. R., Drapeau, M. D., Yazdi, P. G., Shah, K. H., Moise, D. B., Thakar, R. R., Rauser, C. L. & Mueller, L. D. 2002 Evolution of late-life mortality in Drosophila melanogaster. Evolution Int.J.Org.Evolution 56, 1982-1991. Ross, D. A. 1992 The evolution of life histories. Theory and analysis.. New. York: Chapman and Hall. Sear,. R.. 2007. controlling. The. for. impact. of. phenotypic. reproduction. quality. on. reveal. gambian. costs. women:. of. does. reproduction?. Am.J.Phys.Anthropol. 132, 632-641. Sgro, C. M., Geddes, G., Fowler, K. & Partridge, L. 2000 Selection on age at reproduction. in. Drosophila. melanogaster:. female. mating. frequency. as. a. correlated response. Evolution Int.J.Org.Evolution 54, 2152-2155. Smith,. K.. R.,. Mineau,. G.. P.. &. Bean,. L.. L.. 2002. Fertility. and. post-. reproductive longevity. Soc.Biol. 49, 185-205. Sorensen, T. I., Nielsen, G. G., Andersen, P. K. & Teasdale, T. W. 1988 Genetic and environmental influences on premature death in adult adoptees. N.Engl.J.Med. 318, 727-732. Stearns, S. C. 1992 The evolution of life histories. Oxford University Press. Strassmann, B. I. 1997 Polygyny as a risk factor for child mortality among the Dogon. Current Anthropology 38, 688-695. Strassmann, B. I. & Gillespie, B. 2002 Life-history theory, fertility and reproductive success in humans. Proc.Biol.Sci. 269, 553-562. Thomas F., Teriokhin A.T., Renaud F., de Meeûs T. & Guégan J.F. 2000 Human longevity at the cost of reproductive success: evidence from global data. J Evol Biol 13, 409-414. van Dissel, J. T., van Langevelde, P., Westendorp, R. G., Kwappenberg, K. &. 103.

(41) Frolich, M. 1998 Anti-inflammatory cytokine profile and mortality in febrile patients. Lancet 351, 950-953. Westendorp, R. G. & Kirkwood, T. B. 1998 Human longevity at the cost of reproductive success. Nature 396, 743-746. Westendorp, R. G., Langermans, J. A., Huizinga, T. W., Verweij, C. L. & Sturk, A. 1997 Genetic influence on cytokine production in meningococcal disease. Lancet 349, 1912-1913. Westendorp, R. G., van Dunne, F. M., Kirkwood, T. B., Helmerhorst, F. M. & Huizinga, T. W. 2001 Optimizing human fertility and survival. Nat.Med. 7, 873. WHO 2000 Effect of breastfeeding on infant and child mortality due to infectious diseases in less developed countries: a pooled analysis. WHO Collaborative Study Team on the Role of Breastfeeding on the Prevention of Infant Mortality. Lancet 355, 451-455. Wilson, W., Milner, J., Bulkan, J. & Ehlers, P. 2006 Weaning practices of the Makushi of Guyana and their relationship to infant and child mortality: a preliminary assessment of international recommendations. Am.J.Hum.Biol. 18, 312-324. Ziem, J. B., Spannbrucker, N., Magnussen, P., Olsen, A., Amon-Kotey, D. N., Frenzel, K., Nang-Beifubah, A., Westendorp, R. G. & Polderman, A. M. 2005 Oesophagostomum bifurcum-induced nodular pathology in a highly endemic area of Northern Ghana. Trans.R.Soc.Trop.Med.Hyg. 99, 417-422. Zwaan, B., Bijlsma, R. & Hoekstra, R. E. 1995 Direct Selection on Life-Span in Drosophila-Melanogaster. Evolution 49, 649-659.. 104.

(42) 105.

(43)

No results found