ANNALS OF HUMAN BIOLOGY, 1978, VOL. 5, NO. 5, 487--489
Natural selection and birthweight N. B L U R T O N JONES Department of Growth and Development, Institute of Child Health, University of London
Ann Hum Biol Downloaded from informahealthcare.com by Queen's University on 01/06/15 For personal use only.
[Received 23 March 1978; revised 6 May 1978] Summary. Mean birthweight, even before induced births became commonplace, is slightly lower than the birthweight at which perinatal mortality is lowest. This finding, once hard to explain by natural selection, is shown to be exactly in line with predictions from natural selection theory. 1.
Introduction
Karn and Penrose (1952) showed that mean birthweight in man was slightly lower than the "optimum" birthweight, defined as the weight at which perinatal mortality was lowest. This surprised them, since they thought that it was "natural to assume that in consequence of the action of natural selection the mean value of any biological measurement would be the most normal value and associated with the most favourable survival rate". According to evolutionary theory in the 1950s, their surprise was reasonable and the data were a minor embarrassment for the theory of natural selection. However, recent developments in evolutionary theory show the data to be not at all opposed to theory, and indeed precisely in line with what would now be expected. Building on Hamilton's (I964) concept of an individual's inclusive fitness as the measure maximized by natural selection, Trivers (1974) showed that the theory of natural selection predicts a conflict of interests between vertebrate parent and any one offspring. Parent and offspring share only half their genes by common descent. The mother's inclusive fitness is maximized by reducing her care for the first offspring when her influence on its survival has declined, and switching her care to the next offspring. The offspring's fitness is maximized by extracting care from its mother until the benefit to its own survival is outweighed by the detriment (devalued by their coefficient of relatedness) to its siblings. Since the offspring shares all of its genes with itself and only half with its siblings, whereas the mother is equally related to all her offspring, this point will come later for the offspring than for the mother. In fact, Trivers argues that natural selection favours offspring that elicit maternal care until the cost of this care to the mother's inclusive fitness is double the benefit to the offspring's own inclusive fitness. Only beyond this point is its fitness reduced as a result of the reduction in survival of its siblings. It follows from this that the level and duration of parental investment in any one offspring which is optimal for that offspring is greater than the level of investment in that offspring which is optimal for the mother. One would expect natural selection to favour mothers who conserve resources (energy, time, risk of predation etc.) for future offspring (and to the extent that investment in previous offspring still influences their survival, for previous offspring also). Trivers (1974) suggested that weaning conflict and parental pressure against sibling
Ann Hum Biol Downloaded from informahealthcare.com by Queen's University on 01/06/15 For personal use only.
488
Short Reports
rivalry might be results of such conflicting selection. Trivers and Hare (1976) reported a quantitative analysis of reproduction in social insects which supported the theory. The theory of parent-offspring conflict offers a new perspective with which to regard pre-natal development. It would certainly pay an offspring to evolve mechanisms ensuring that its birthweight was very near that which minimized perinatal mortality. But it would pay a mother to give birth to a baby of a somewhat lower weight, given that investment in carrying and nourishing this baby may reduce the possible investment in previous and subsequent offspring. Direct evidence that the mother's reproductive success is aided by conserving resources from her current fetus would be valuable. One type of evidence might concern maternal mortality. However, in a species with strong parental investment, death of the mother would be as disadvantageous to the inclusive fitness of a particular offspring as to the mother. Evidence about influences upon the mother's future production of offspring and their survivorship would be very hard to attain because of the need to take adverse circumstances and their variation into account. There is evidence that human birthweight is reduced by undernutrition in the third trimester of pregnancy, and an indication that undernutrition shortens gestation (Stein, Susser, Saenger and Marolla, 1975). There is evidence that the mother asserts a restraining influence on birthweight (Tanner, 1974). If, as seems reasonable, we may assume that conserving resources from the present offspring increases the chances of successfully raising subsequent offspring, we should expect the birthweight optimal for the mother's inclusive fitness to be lower than the birthweight optimal for the offspring's inclusive fitness. Birthweight should then be a compromise between the baby's optimum and the mother's optimum. Karn and Penrose's data are exactly in line with this prediction (and were reported long before the recent fashion for induced births). Karn and Penrose present data from Hoseman (1950) in Germany which also show a mean birthweight slightly lower than the birthweight that carries minimal mortality for the foetus. Parent-offspring conflict thus transforms the discrepancy reported by Karn and Penrose from being a slight embarrassment for the theory of natural selection into a surprisingly close fit with evolution theory.
Acknowledgments I am grateful to R. L. Trivers for suggesting that I pursue parent-offspring conflict prenatally. This note is part of the work of our Social Science Research Council Research Programme on the Biology and Psychology of Early Mother-Infant Interaction.
References Hamilton, W. D. (1964). The genetic theory of social behaviour I, II. Journal of Theoretical Biology, 7, 1-52. Hoseman, H. (1950). Kindlich Masse und Neugeborenesterblichkeit. Naturwissenschaften, 37, 409416. Karn, M. N., and Penrose, L. S. (1952). Birth weight and gestation time in relation to maternal age, parity and infant survival. Annals of Eugenics, 16, 147-164. Stein, Z., Susser, M., Saenger, G., and Marolla, F. (1975).Famine and Human Development. London: Oxford University Press. Tanner, J. M. (1974). Variability of growth and maturity in newborn infants. In The Effect of the Newborn on its Caregiver, eds. Lewis, M. and Rosenblum, L. New York: John Wiley. Trivers, R. L. (1974). Parent-offspring conflict. American Zoologist, 14, 247-262.
Short Reports Trivers, R. L., and Hare, H. (1976). Haplodiploidy and the evolution of social insects. 249-263.
489
Science, 191,
Address correspondence to: N. Blurton Jones, Department of Growth and Development, Institute of Child Health, 30 Guilford Street, London W C I N 1EH.
Ann Hum Biol Downloaded from informahealthcare.com by Queen's University on 01/06/15 For personal use only.
Zusammenfassung. Das mittlere Geburtsgewicht ist etwas niedriger als das Geburtsgewicht, bei dem die perinatale Sterblichkeit am niedrigsten ist, auch bevor die induzierten Geburten allgemein fiblich wurden. Es wird gezeigt, dab dieses Ergebnis, das frfiher durch natiirliche Selektion schwer zu erkl/iren war, gut tibereinstimmt mit Voraussagen nach der modernen Theorie der nat/irlichen Selektion. Rdsum6. Le poids de naissance moyen, m~me avant que l'accouchement provoqud soit devenu commun, dtait Idg~rement inf6rieur au poids de naissance pour lequel la mortalitd pdrinatale dtait la plus basse. Cette ddcouverte, qui a paru difficile ~_expliquer par la s61ection naturelle, est montrde 6tre exactement conforme aux prddictions de la thdorie moderne de la sdlection naturelle.
A...B.
2K
Natural selection and birthweight N. B L U R T O N JONES Department of Growth and Development, Institute of Child Health, University of London
Ann Hum Biol Downloaded from informahealthcare.com by Queen's University on 01/06/15 For personal use only.
[Received 23 March 1978; revised 6 May 1978] Summary. Mean birthweight, even before induced births became commonplace, is slightly lower than the birthweight at which perinatal mortality is lowest. This finding, once hard to explain by natural selection, is shown to be exactly in line with predictions from natural selection theory. 1.
Introduction
Karn and Penrose (1952) showed that mean birthweight in man was slightly lower than the "optimum" birthweight, defined as the weight at which perinatal mortality was lowest. This surprised them, since they thought that it was "natural to assume that in consequence of the action of natural selection the mean value of any biological measurement would be the most normal value and associated with the most favourable survival rate". According to evolutionary theory in the 1950s, their surprise was reasonable and the data were a minor embarrassment for the theory of natural selection. However, recent developments in evolutionary theory show the data to be not at all opposed to theory, and indeed precisely in line with what would now be expected. Building on Hamilton's (I964) concept of an individual's inclusive fitness as the measure maximized by natural selection, Trivers (1974) showed that the theory of natural selection predicts a conflict of interests between vertebrate parent and any one offspring. Parent and offspring share only half their genes by common descent. The mother's inclusive fitness is maximized by reducing her care for the first offspring when her influence on its survival has declined, and switching her care to the next offspring. The offspring's fitness is maximized by extracting care from its mother until the benefit to its own survival is outweighed by the detriment (devalued by their coefficient of relatedness) to its siblings. Since the offspring shares all of its genes with itself and only half with its siblings, whereas the mother is equally related to all her offspring, this point will come later for the offspring than for the mother. In fact, Trivers argues that natural selection favours offspring that elicit maternal care until the cost of this care to the mother's inclusive fitness is double the benefit to the offspring's own inclusive fitness. Only beyond this point is its fitness reduced as a result of the reduction in survival of its siblings. It follows from this that the level and duration of parental investment in any one offspring which is optimal for that offspring is greater than the level of investment in that offspring which is optimal for the mother. One would expect natural selection to favour mothers who conserve resources (energy, time, risk of predation etc.) for future offspring (and to the extent that investment in previous offspring still influences their survival, for previous offspring also). Trivers (1974) suggested that weaning conflict and parental pressure against sibling
Ann Hum Biol Downloaded from informahealthcare.com by Queen's University on 01/06/15 For personal use only.
488
Short Reports
rivalry might be results of such conflicting selection. Trivers and Hare (1976) reported a quantitative analysis of reproduction in social insects which supported the theory. The theory of parent-offspring conflict offers a new perspective with which to regard pre-natal development. It would certainly pay an offspring to evolve mechanisms ensuring that its birthweight was very near that which minimized perinatal mortality. But it would pay a mother to give birth to a baby of a somewhat lower weight, given that investment in carrying and nourishing this baby may reduce the possible investment in previous and subsequent offspring. Direct evidence that the mother's reproductive success is aided by conserving resources from her current fetus would be valuable. One type of evidence might concern maternal mortality. However, in a species with strong parental investment, death of the mother would be as disadvantageous to the inclusive fitness of a particular offspring as to the mother. Evidence about influences upon the mother's future production of offspring and their survivorship would be very hard to attain because of the need to take adverse circumstances and their variation into account. There is evidence that human birthweight is reduced by undernutrition in the third trimester of pregnancy, and an indication that undernutrition shortens gestation (Stein, Susser, Saenger and Marolla, 1975). There is evidence that the mother asserts a restraining influence on birthweight (Tanner, 1974). If, as seems reasonable, we may assume that conserving resources from the present offspring increases the chances of successfully raising subsequent offspring, we should expect the birthweight optimal for the mother's inclusive fitness to be lower than the birthweight optimal for the offspring's inclusive fitness. Birthweight should then be a compromise between the baby's optimum and the mother's optimum. Karn and Penrose's data are exactly in line with this prediction (and were reported long before the recent fashion for induced births). Karn and Penrose present data from Hoseman (1950) in Germany which also show a mean birthweight slightly lower than the birthweight that carries minimal mortality for the foetus. Parent-offspring conflict thus transforms the discrepancy reported by Karn and Penrose from being a slight embarrassment for the theory of natural selection into a surprisingly close fit with evolution theory.
Acknowledgments I am grateful to R. L. Trivers for suggesting that I pursue parent-offspring conflict prenatally. This note is part of the work of our Social Science Research Council Research Programme on the Biology and Psychology of Early Mother-Infant Interaction.
References Hamilton, W. D. (1964). The genetic theory of social behaviour I, II. Journal of Theoretical Biology, 7, 1-52. Hoseman, H. (1950). Kindlich Masse und Neugeborenesterblichkeit. Naturwissenschaften, 37, 409416. Karn, M. N., and Penrose, L. S. (1952). Birth weight and gestation time in relation to maternal age, parity and infant survival. Annals of Eugenics, 16, 147-164. Stein, Z., Susser, M., Saenger, G., and Marolla, F. (1975).Famine and Human Development. London: Oxford University Press. Tanner, J. M. (1974). Variability of growth and maturity in newborn infants. In The Effect of the Newborn on its Caregiver, eds. Lewis, M. and Rosenblum, L. New York: John Wiley. Trivers, R. L. (1974). Parent-offspring conflict. American Zoologist, 14, 247-262.
Short Reports Trivers, R. L., and Hare, H. (1976). Haplodiploidy and the evolution of social insects. 249-263.
489
Science, 191,
Address correspondence to: N. Blurton Jones, Department of Growth and Development, Institute of Child Health, 30 Guilford Street, London W C I N 1EH.
Ann Hum Biol Downloaded from informahealthcare.com by Queen's University on 01/06/15 For personal use only.
Zusammenfassung. Das mittlere Geburtsgewicht ist etwas niedriger als das Geburtsgewicht, bei dem die perinatale Sterblichkeit am niedrigsten ist, auch bevor die induzierten Geburten allgemein fiblich wurden. Es wird gezeigt, dab dieses Ergebnis, das frfiher durch natiirliche Selektion schwer zu erkl/iren war, gut tibereinstimmt mit Voraussagen nach der modernen Theorie der nat/irlichen Selektion. Rdsum6. Le poids de naissance moyen, m~me avant que l'accouchement provoqud soit devenu commun, dtait Idg~rement inf6rieur au poids de naissance pour lequel la mortalitd pdrinatale dtait la plus basse. Cette ddcouverte, qui a paru difficile ~_expliquer par la s61ection naturelle, est montrde 6tre exactement conforme aux prddictions de la thdorie moderne de la sdlection naturelle.
A...B.
2K
