Hum. Reprod. Advance Access originally published online on August 6, 2008
Human Reproduction 2008 23(10):2387-2389; doi:10.1093/humrep/den305
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Letters to the Editor |
Why twin pregnancies are more successful at advanced than young maternal age? A potential role of ‘terminal reproductive investment’
Section of Ecology, Department of Biology, University of Turku, FI-20014 Turku, Finland
Correspondence address. Tel: +358-2-333-6559; Fax: +358-2-333-6550; E-mail: samuli.helle{at}utu.fi
The article by Delbaere et al. ‘Perinatal outcome of twin pregnancies in women of advanced age’, in Hum Reprod (2008), showed that irrespective of reproductive techniques, socio-economic status and the zygosity of twins, perinatal outcome of twin pregnancies is more favourable in primiparous women aged 35 or over compared with primiparous women aged 25–29 years. As stated by the authors themselves, this is a paradoxical phenomenon, because singletons born to older mothers are commonly at disadvantage (Tarin et al., 1998
). Both the physiological mechanisms and the ultimate causes behind this phenomenon remain unknown. Here, I propose one potential resolution, based on evolutionary theory, that might help shed light on the question why multiple pregnancies seem to have better outcome among older than young mothers.
Evolutionary theory predicts that in species reproducing many times during their lifetime, reproductive effort (the proportion of parental resources invested in offspring from conception to independence) should increase with advancing age, as ageing reduces their residual reproductive value due to the decreasing future probability of reproduction and survival (Clutton-Brock, 1984). This age-dependency of reproductive effort should eventually manifested itself as a terminal reproductive effort (thus, the term ‘terminal investment hypothesis’), where individuals invest heavily in their last reproductive event because there is no future reproduction to loose. Women fit well with the assumptions of this hypothesis, because menopause sets a clear end-point to their fertility, making terminal reproductive effort a potentially advantageous reproductive strategy.
But how well this hypothesis fit with our knowledge on human multiple births and how might it advance our understanding of the age-dependent outcomes of multiple births? First, advanced maternal age has been regarded as one of the most important factors increasing the rate of heritable multiple births (e.g. dizygotic twins and trizygotic triplets) (Bulmer, 1970; Bortolus et al., 1999; Hoekstra et al., 2008). For example, between the ages 15 and 37, the dizygotic twinning rate has been reported to show more than a 4-fold increase (Bulmer, 1970). High parity has also been suggested to have an independent positive effect on dizygotic twinning rates (Bulmer, 1970). Both advanced maternal age and high parity are relevant to the terminal investment hypothesis, as they both point towards the end of a woman's reproductive lifespan: an age close to menopause represents a physiological constraint on fecundity, whereas high parity may indicate that a desired or, given an environmental-context, a maximum family size is almost accomplished. Second, multiple births have been considered to result from natural selection on more relaxed screening mechanisms of, for example, developing multiple embryos with increasing maternal age (Anderson, 1990; Forbes, 1997; Ball and Hill, 1999). This idea was originally developed to suggest that multiple births are, in terms of maternal evolutionary fitness, harmful side effects of such screening mechanisms. However, later studies have indicated that such mechanisms, if responsible for polyovulation, may have actually been selected for as older mothers can increase their reproductive effort and fitness by the production of multiple births (Lummaa et al., 1998; Helle et al., 2004). Third, mothers have been reported to be more likely to completely terminate their reproductive career after delivering a twins compared with mothers delivering singletons only (Lummaa, 2001; Pison and Couvert, 2004).
These findings suggest that older mothers may increase their reproductive effort by producing multiples. However, in order to be a strategy favoured by natural selection, the amount of investment in multiples conceived should also increase with the increasing maternal age (Clutton-Brock, 1984). The current evidence supports this. First, survival to independence or adulthood is an important proxy of post-partum maternal investment in offspring. Studies on the survival of twins compared with singletons have shown that even in premodern times twin births produced more adult offspring than singleton births (Lummaa et al., 2001; Helle et al., 2004) and that the survival of multiples is improved in older mothers compared with younger ones in both historical and contemporary populations (Voland and Gabler, 1994; Misra and Ananth, 2002; Zhang et al., 2002; Imaizumi, 2003; Salihu et al., 2004; Luke and Brown, 2007). Second, in contrast to singleton deliveries, twins born to older mothers are not in higher risk of very preterm birth compared to younger mothers (Blickstein et al., 2001; Zhang et al., 2002; Branum and Schoendorf, 2005; Delbaere et al., 2008), and older mothers have been reported to give birth to heavier triplets than the younger mothers (Keith et al., 2004; Blickstein et al., 2005). Third, no adverse long-term effects of being a twin versus being a singleton on the adult-life reproductive performance and survival have currently been reported (Vagero and Leon, 1994; Christensen et al., 1998, 2001). In sum, these findings indicate that mothers invest more in multiple deliveries as they approach the end of their reproductive lives.
Therefore, the higher incidence of multiple births and their more favourable outcomes with advanced maternal age may, at least partly, be related to the increased reproductive effort by older mothers, as predicted by the terminal investment hypothesis. It, however, still remains an unanswered question why naturally occurring multiple births are rather rare events and not manifested by all reproducing old mothers? It is known that many more multiple conceptions are taking place than that are born (the ‘vanishing twin’ phenomenon; Landy and Keith, 1998) and that mothers delivering multiples are generally in good physiological condition and taller (Campbell et al., 1974; Bortolus et al., 1999; Madrigal et al., 2001; Sear et al., 2001; Basso et al., 2004; Reddy et al., 2005). This suggests that many women posses a genetic propensity to multiple births, potentially indicating a historical selection pressure for polyovulation, which is sensitive to maternal nutritional status and, hence, expressed mainly among those mothers who have abundant resources to increase their reproductive effort. Such a strategy has likely been adaptive, because multiple births have hardly been favoured in environments of low resource availability and poor offspring survival (Lummaa et al., 1998). In addition, it is problematic why mothers having singletons only, who compromise the majority of the populations, do not generally seem to show an increased reproductive effort with age (Fessler et al., 2005). More studies are needed thus to elaborate the evolutionary roots of multiple births in humans.
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