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Thursday, February 08, 2007
At his personal website, our co-blogger Matt recently posted on a conference presentation by Bodnar, Simhan, and colleagues -- details here -- which shows a seasonal pattern of preterm births in the US. Simhan suggests that this new study is the most rigorous such study in an industrialized country, but there have been several other such studies. Lee et al. (2006) review the literature on preterm birth seasonality in the developing and developed countries, and present a new study of their own that examined the London-area population (N=482,765). In any event, is there something adaptive about this pattern, as Matt asks? I think so, and the answer comes from life history theory (Roff 2002 provides an overview of the field, while Roff 2007 discusses how genomics can illuminate life history investigations). In brief, it is possible to view preterm birth as a facultative "desertion" strategy that mothers use when they perceive environmental cues that signal rough times ahead for their infant offspring. But before developing an explanation, let's first review the relevant evidence. From the Lee et al. (2006, p.1282) summary on the developed countries:
Using secondary data analysis, two developed countries reported similar preterm birth seasonality.[14,21,22] In the USA and Japan, the pattern was annual, with the highest proportions and risk occurring twice a year: once in summer and again in winter. The lowest risk was observed in spring and autumn.
One study from the USA reported no seasonality of preterm birth.[23] This study compared preterm birth rates from May to October with those from November to April for 1983-85 in a northern Californian population and found no difference in spontaneous preterm birth proportions.
Add to that the new study by Bodnar, Simhan, and colleagues on the most risky season being Winter (though not Summer as well). Add also the novel study in Lee et al. (2006), which also found that preterm births were more likely among Winter (but not Summer) births in the London area. As for the developing countries (same page as above):
In the developing countries, all three studies that were located reported a seasonality of preterm birth using their own definitions of seasons. In Bangladesh,[24] the lowest proportion of preterm births occurred during winter (3.6%), followed by summer (5.5%) and monsoon (6.0%) season. The highest proportion of preterm births was observed in autumn (8.3%).
In Gambia, two seasons were reported.[13] Preterm birth proportions were found to peak twice a year: once at the beginning of the hungry season in July and again towards the end of the hungry season in October.
Harare, Zimbabwe, was reported to experience four seasons.[25] Births in the early dry season were three times more likely to be preterm compared with those during the late rainy season (OR 2.9, 95% CI 1.65-5.2). No other seasonal differences in the risk of preterm birth between seasons were found.
The common denominator appears to be that when environmental quality predictably becomes much worse, preterm births become more common. In the developed world, we know that Winter is the flu season when infection is more likely. Studies of seasonality of disease in Bangladesh suggest that the low-point for preterm births in Bangladesh occurs with the low-point for nasty infectious diseases such as malaria (Rahman et al. 2006; free text), cholera (Alam et al. 2006; free text), and diarrhea (see the abstract of this study), all of which reach their nadir in Winter. Each of these diseases peaks in various non-Winter seasons, but both malaria and cholera appear to peak in Autumn just like preterm births. As for variable environmental quality in Gambia, the name of "the hungry season" speaks for itself.
Why might something like an infection cause the mother to deliver a preterm baby? Consider that if the mother is infected, it's also likely that the fetus will become infected as well, either in the womb, on the way through the birth canal, or what have you. An offspring that has been parasitized before even being born is clearly of lower quality, so perhaps once the mother's body recognizes it has been parasitized, it decides to in effect abandon the child -- since delivering it preterm, in the absence of superior medical care, is tantamount to aborting it -- and start over again. Note that humans are capable of mating, conceiving, and giving birth to offspring year-round, so the benefit from a mother cutting her losses and beginning anew would not be outweighed by a large cost. Assume a mother in the developed countries essentially aborts the child in Winter; if she mates right away, she can deliver another child by the coming Autumn, before the worst period of risk of infection sets in. Alternatively, she could wait just 6 months, mate in Summer, and deliver a child by the following Spring after the worst period of risk of infection had passed.
Hunter-gatherers tend to space their births four years apart because their way of life cannot sustain a family of, say, 10 offspring. Even among most agricultural populations during most of human history, you figure 4 or 5 offspring would have been on the high-end of average -- thus, forgoing child-rearing by waiting just 6 months is not going to impinge much on the mother's lifetime fecundity, and will certainly boost the fitnesses of the surviving offspring with respect to coping with pathogens. So, making the switch to desertion of her offspring will not likely incur substantial costs, which in any case would likely be outweighed by the benefit of having non-parasitized offspring.
But is there any independent evidence that this sort of thing happens? For birds, at least, the answer is "yes." Roff (2002) cites a study by Oppliger et al. (1994) which demonstrated that great tit mothers were more likely to desert their nest if it had been infested by an ectoparasite (the hen flea). Something similar occurs among bird species subject to brood parasitism, whereby the mother of another species places her own egg(s) in the nest of the host bird species, which clearly imposes costs on the latter since she expends energy and resources in raising an unrelated offspring. A review by Hosoi & Rothstein (2000) shows that species that have spent longer evolutionary periods of time with the parasitic cowbirds are more likely to desert their nest after being exposed to a particular cue of parasitism than are those who have been more recently troubled by the cowbirds' ways. There are some important details that are, however, irrelevant to the discussion of human desertion: for example, it seems that the host bird mothers pay more attention to the presence of cowbird mothers nearby, rather than discriminate between "self" eggs and "other" eggs. The point is simply that nest desertion shows signs of being an adaptive response to parasitism. Also, one strategy available to birds is to eject the "other" egg from their nest, but humans cannot so easily purge their body of pathogens.
So, does the seasonality of human preterm births permit an adaptive explanation? The evidence could certainly be stronger, but based on a consideration of the predictable seasonal patterns in environmental quality, the trade-offs involved in "deserting" an infant by delivering it preterm, and evidence from other animals such as birds subject to various types of parasitism, the hypothesis seems on the right track, at least sufficiently so that future studies should incorporate more of a life history perspective. For example, Pike's (2005) discussion of life history and preterm births shows how such theoretical approaches can clear up confusion in the field of medicine, in which evolution tends not to occupy a central role.
References
Alam, M, NA Hasan, A Sadique, NA Bhuiyan, KU Ahmed, and others (2006). Seasonal Cholera Caused by Vibrio cholerae Serogroups O1 and O139 in the Coastal Aquatic Environment of Bangladesh. Applied and Environmental Microbiology, 72, 4096-104.
Hosoi, SA & SI Rothstein (2000). Nest desertion and cowbird parasitism: evidence for evolved responses and evolutionary lag. Animal Behaviour, 59, 823-40.
Lee, SJ, PJ Steer, & V Filippi (2006). Seasonal patterns and preterm birth: a systematic review of the literature and an analysis in a London-based cohort. BJOG, 113, 1280-88.
Oppliger, A, H Richner, & P Christe (1994). Effect of an ectoparasite on lay date, nest-site choice, desertion, and hatching success in the great tit (Parus major). Behavioral Ecology, 5, 130-4. Cited in Roff (2002), p. 415.
Pike, IL (2005). Maternal stress and fetal responses: Evolutionary perspectives on preterm delivery. American Journal of Human Biology, 17, 55-65.
Rahman, A, F Kogan, & L Roytman (2006). Analysis of malaria cases in Bangladesh with remote sensing data. The American Journal of Tropical Medicine and Hygiene, 74, 17-9.
Roff, DA (2002). Life history evolution. Sunderland: Sinauer Associates.
Roff, DA (2007). Contributions of genomics to life-history theory. Nature Reviews Genetics, 8, 116-25.
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