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• W2055750996 abstract "Despite popular misconceptions, natural selection does operate in modern human populations. New studies even show that changes associated with modernization are deeply reshaping selection pressures and, perhaps, bits of our biological nature. Despite popular misconceptions, natural selection does operate in modern human populations. New studies even show that changes associated with modernization are deeply reshaping selection pressures and, perhaps, bits of our biological nature. Thomas Robert Malthus (1766–1834) understood well how fertility in excess of self-replacement would rapidly overcrowd a country and lead to the depletion of its limited resources, if it weren’t for the ‘checks’ (e.g., high death rates) keeping populations within certain limits. He even wrote a whole essay [1Malthus T.R. An Essay on the Principle of Population, Oxford World’s Classic 1993 edition. Oxford University Press, Oxford1798Google Scholar] on the topic that was a source of inspiration to Charles Darwin to propose his theory of evolution by natural selection. What Darwin may not have foreseen, though, is that a sharp decline in fertility and mortality can also fuel the evolutionary machinery. The confirmation is now provided by a study published in this issue of Current Biology: Courtiol and colleagues [2Courtiol A. Rickard I.J. Lummaa V. Prentice A.M. Fulford A.J.C. Stearns S.C. The demographic transition influences variance in fitness and selection on height and BMI in rural Gambia.Curr. Biol. 2013; 23: 884-889Abstract Full Text Full Text PDF PubMed Scopus (22) Google Scholar] show that a phenomenon called ‘demographic transition’ — the decline of fertility and mortality rates in societies that undergo modernization — modified natural selection on body shape in an African population. To better appreciate this contribution, let’s first overview the state of our knowledge on contemporary evolution. Conventional wisdom often asserts that biological evolution came to a halt in humans. Thanks to progress in medicine, nutrition, birth control and freedom of family planning, our children survive better and we can say ‘goodbye!’ to natural fertility without compromising too much of our genetic descent (i.e. our Darwinian fitness determined by our survival, mating and reproduction and that of our offspring). As a consequence, natural selection could not possibly be happening in modern societies, right? Wrong! Natural selection occurs whenever there is variance in fitness and whenever this variance covaries with observable characters (phenotypes). These are two conditions that are not very hard to find in contemporary humans [3Courtiol A. Pettay J.E. Jokela M. Rotkirch A. Lummaa V. Natural and sexual selection in a monogamous historical human population.Proc. Natl. Acad. Sci. USA. 2012; 109: 8044-8049Crossref PubMed Scopus (68) Google Scholar, 4Stearns S.C. Byars S.G. Govindaraju D.R. Ewbank D. Measuring selection in contemporary human populations.Nat. Rev. Genet. 2010; 11: 611-622Crossref PubMed Google Scholar, 5Byars S.G. Ewbank D. Govindaraju D.R. Stearns S.C. Natural selection in a contemporary human population.Proc. Natl. Acad. Sci. USA. 2010; 107: 1787-1792Crossref PubMed Scopus (121) Google Scholar]. Selection, however, is not evolution, and the latter requires an extra condition to become a reality: the existence of genetic variation (heritability) in traits under selection. That too is apparently not so rare in our species [4Stearns S.C. Byars S.G. Govindaraju D.R. Ewbank D. Measuring selection in contemporary human populations.Nat. Rev. Genet. 2010; 11: 611-622Crossref PubMed Google Scholar, 5Byars S.G. Ewbank D. Govindaraju D.R. Stearns S.C. Natural selection in a contemporary human population.Proc. Natl. Acad. Sci. USA. 2010; 107: 1787-1792Crossref PubMed Scopus (121) Google Scholar, 6Pettay J.E. Kruuk L.E.B. Jokela J. Lummaa V. Heritability and genetic constraints of life-history trait evolution in preindustrial humans.Proc. Natl. Acad. Sci. USA. 2005; 102: 2838-2843Crossref PubMed Scopus (129) Google Scholar]. Moreover, evidence is accumulating that evolution can be rapid in the wild, even in species with a slower pace of life than microbes or flies [7Coltman D.W. O’Donoghue P. Jorgenson J.T. Hogg J.T. Strobeck C. Festa-Bianchet M. Undesirable evolutionary consequences of trophy hunting.Nature. 2003; 426: 655-658Crossref PubMed Scopus (567) Google Scholar]. Humans are no exception. For example, a recent study [8Milot E. Mayer F.M. Nussey D.H. Boisvert M. Pelletier F. Réale D. Evidence for evolution in response to natural selection in a contemporary human population.Proc. Natl. Acad. Sci. USA. 2011; 108: 17040-17045Crossref PubMed Scopus (79) Google Scholar] of a contemporary human population revealed evolutionary change in reproductive traits over a mere 140 years. With advances in statistical tools comes the opportunity to explore not only the patterns produced by recent evolution — such as the geographical distribution of genetic variants conferring adaptation to altitude in mountain-dwelling humans [9Wills C. Rapid recent human evolution and the accumulation of balanced genetic polymorphisms.High Alt. Med. Biol. 2011; 12: 149-155Crossref PubMed Scopus (9) Google Scholar] — but also the process of evolution itself, generation per generation. This has increased awareness that ecological and evolutionary processes can interact to shape demographic and phenotypic trends in contemporary natural populations [10Carroll S.P. Hendry A.P. Reznick D.N. Fox C.W. Evolution on ecological time-scales.Funct. Ecol. 2007; 21: 387-393Crossref Scopus (469) Google Scholar]. The demographic transition is one major step in the history of modern human populations that impacts evolutionary processes. It typically begins with a sharp decrease in mortality arising from technological and societal improvements in living conditions, such as hygiene, disease prevention and health care, followed by a decrease in fertility. Typically this causes population size to grow then to stabilize or even decline towards the end of the transition. While the reasons for the decrease in mortality are well understood, the decrease in fertility still puzzles demographists, social scientists and biologists. Apart from purely sociological explanations, such as adherence to contraceptive use, three evolutionary hypotheses have been proposed to explain the reduction in fertility [11Borgerhoff Mulder M. The demographic transition: are we any closer to an evolutionary explanation?.Trends Ecol. Evol. 1998; 13: 266-270Abstract Full Text Full Text PDF PubMed Scopus (186) Google Scholar, 12Newson L. Postmes T. Lea S.E.G. Webley P. Why are modern families small? Toward an evolutionary and cultural explanation for the demographic transition.Pers. Soc. Psychol. Rev. 2005; 9: 360-375Crossref PubMed Scopus (99) Google Scholar]: first, individuals might be trading-off offspring quantity vs. quality to maximize Darwinian fitness and that a smaller family is optimal in the modern environment (behavioural ecology perspective); second, reduced fertility might be a maladaptive response to an environment changing radically (evolutionary psychology perspective); and third, the influence of kin on individual reproductive decisions may have decreased with the widening of social networks, limiting the incentives for having big families (cultural transmission hypothesis). All of these hypotheses rely on the action of mechanisms (cognitive, physiological) that influence current reproductive decisions but have evolved in the past. However, much less attention has been paid to how contemporary evolution interacts with the demographic transition (Figure 1). Courtiol and colleagues [2Courtiol A. Rickard I.J. Lummaa V. Prentice A.M. Fulford A.J.C. Stearns S.C. The demographic transition influences variance in fitness and selection on height and BMI in rural Gambia.Curr. Biol. 2013; 23: 884-889Abstract Full Text Full Text PDF PubMed Scopus (22) Google Scholar] examined how the transition modulated natural selection on human phenotypes in two rural villages in Gambia (Figure 2). One of the main strengths of their study is the exceptional data set encompassing a 55-year interval across the demographic transition. Life history events (birth, reproduction and death) and morphometric measurements (height, weight) were available from regular medical follow-ups on women, and there were data on neonate health. Two common challenges in evolutionary studies are censoring (e.g., individuals with incomplete reproduction by the end of the study period) and non-random mortality with respect to phenotype [13Hadfield J.D. Estimating evolutionary parameters when viability selection is operating.Proc. R. Soc. Lond. B Bio. 2008; 275: 723-734Crossref PubMed Scopus (153) Google Scholar]. The authors tackle these using an original statistical approach to follow selection in real-time (year after year) while controlling for age-related changes in traits and non-independence due to repeated fitness measurement on the same individuals. This way, rapid changes in selection that could easily go undetected using classic fitness proxies such as lifetime reproductive success are more discernible. Measuring natural selection is not a simple task, however. The most common metrics are the covariance between relative fitness and a phenotypic trait — measuring the strength of selection on the trait — and the variance (among individuals) in relative fitness, also known as the ‘opportunity for selection’. While the latter is generally viewed as setting an upper limit to the former, how these two quantities are correlated and whether they provide complementary information are currently debated among evolutionary biologists [14Krakauer A. Webster M. Duval E. Jones A. Shuster S. The opportunity for sexual selection: not mismeasured, just misunderstood.J. Evol. Biol. 2011; 24: 2064-2071Crossref PubMed Scopus (91) Google Scholar, 15Pelletier F. Coulson T. A new metric to calculate the opportunity for selection quantitative characters.Evol. Ecol. Res. 2012; 14: 729-742Google Scholar]. Thus, studies exploring the links between these measurements can bring insight into the modus operandi of natural selection. This is the approach adopted by Courtiol and colleagues [2Courtiol A. Rickard I.J. Lummaa V. Prentice A.M. Fulford A.J.C. Stearns S.C. The demographic transition influences variance in fitness and selection on height and BMI in rural Gambia.Curr. Biol. 2013; 23: 884-889Abstract Full Text Full Text PDF PubMed Scopus (22) Google Scholar]. The variance in relative fitness in the two Gambian villages declined during the demographic transition. However, this trend hides contrasting effects on fitness components. The variance in relative child survival was fluctuating at the beginning of the study but dropped down near zero afterwards when the villages experienced an improvement of medical care following the establishment of a clinic in 1974. In contrast, the variance in relative fertility initially decreased and then rebounded after 1974 to reach a maximum after the year 2000. Such inverse trends in the opportunity for selection mediated through survival and fertility could be a general feature of societies in demographic transition [16Moorad J.A. A demographic transition altered the strength of selection for fitness and age-specific survival and fertility in a 19th century American population.Evolution. 2013; https://doi.org/10.1111/evo.12023Crossref Scopus (28) Google Scholar] and were also reported for other populations (at least over part of their transition, e.g. [17Terrenato L. Ulizzi L. San Martini A. The effects of demographic transition on the opportunity for selection: changes during the last century in Italy.Ann. Hum. Genet. 1979; 42: 391-399Crossref PubMed Scopus (31) Google Scholar]). Things get fascinating when morphological traits are thrown into the picture. The authors showed that selection on height and body-mass index has changed between 1955 and 2010 in the two Gambian villages [2Courtiol A. Rickard I.J. Lummaa V. Prentice A.M. Fulford A.J.C. Stearns S.C. The demographic transition influences variance in fitness and selection on height and BMI in rural Gambia.Curr. Biol. 2013; 23: 884-889Abstract Full Text Full Text PDF PubMed Scopus (22) Google Scholar]: smaller and chubbier (higher body-mass index) women had the initial fitness advantage but the trend reversed progressively in favour of those taller and thinner. Both demography per se and environmental changes underlying the transition modified selection in complex ways (Figure 1). Regarding demography, the reduction in survival variance, thus in the opportunity for selection, favoured a general decline in the strength of selection on body shape, with a limited counteracting effect of increasing variance in fertility. The environment reversed the direction of selection, specifically of the relationship between fertility and both height and body-mass index, but the precise environmental factors involved in this shift remain to be investigated. Thus, the two phenomena had complementary effects on selection. The proportion of the total variation in the strength of selection explained by the demographic transition was moderate (up to 19%). Therefore, other unmeasured factors manifestly contributed to year-to-year fluctuations in selection. Nevertheless, the study by Courtiol and colleagues [2Courtiol A. Rickard I.J. Lummaa V. Prentice A.M. Fulford A.J.C. Stearns S.C. The demographic transition influences variance in fitness and selection on height and BMI in rural Gambia.Curr. Biol. 2013; 23: 884-889Abstract Full Text Full Text PDF PubMed Scopus (22) Google Scholar] shows that rapid demographic changes in modern human populations can modify selection on phenotypes, in this case body shape. Another recently published important study [16Moorad J.A. A demographic transition altered the strength of selection for fitness and age-specific survival and fertility in a 19th century American population.Evolution. 2013; https://doi.org/10.1111/evo.12023Crossref Scopus (28) Google Scholar] examined in depth the dynamics of selection on age-specific mortality and fertility (vital rates) and fitness itself during the demographic transition (Figure 1). The author [16Moorad J.A. A demographic transition altered the strength of selection for fitness and age-specific survival and fertility in a 19th century American population.Evolution. 2013; https://doi.org/10.1111/evo.12023Crossref Scopus (28) Google Scholar] shows how decreasing population growth rate increases the contribution of fertility to the variance in relative fitness, boosting selection on fertility. Importantly, this process is expected to slow down (resist) the pace of the demographic transition when fertility is heritable. Ultimately, the demographic transition is just one amongst the panoply of new playgrounds offered by the modern human life-style to natural selection. Who knows what other playgrounds can emerge from features such as exposure to new synthetic molecules, large-scale mobility, changing climate, and so forth. And the traits playing the game could be as diverse as cholesterol levels, age at reproduction, body shape, personality, immune defence, or even political choices [2Courtiol A. Rickard I.J. Lummaa V. Prentice A.M. Fulford A.J.C. Stearns S.C. The demographic transition influences variance in fitness and selection on height and BMI in rural Gambia.Curr. Biol. 2013; 23: 884-889Abstract Full Text Full Text PDF PubMed Scopus (22) Google Scholar, 4Stearns S.C. Byars S.G. Govindaraju D.R. Ewbank D. Measuring selection in contemporary human populations.Nat. Rev. Genet. 2010; 11: 611-622Crossref PubMed Google Scholar, 5Byars S.G. Ewbank D. Govindaraju D.R. Stearns S.C. Natural selection in a contemporary human population.Proc. Natl. Acad. Sci. USA. 2010; 107: 1787-1792Crossref PubMed Scopus (121) Google Scholar, 18Ferreira Z. Seixas S. Andrés A.M. Kretzschmar W.W. Mullikin J.C. Cherukuri P.F. Cruz P. Swanson W.J. Clark A.G. Green E.D. Reproduction and immunity-driven natural selection in the human WFDC locus.Mol. Biol. Evol. 2013; 30: 938-950Crossref PubMed Scopus (15) Google Scholar, 19Fowler J.H. Baker L.A. Dawes C.T. Genetic variation in political participation.Am. Polit. Sci. Rev. 2008; 102: 233-248Crossref Scopus (257) Google Scholar]. Understanding how culture and modern life-style lead to new selective environments should provide major insights into human evolution. The next challenge will be to assess whether selection and evolution can have any concrete impact on human affairs such as public health, demographic forecasts or mate choice. For instance, lingering effects of the demographic transition could impact on the evolution of senescence [16Moorad J.A. A demographic transition altered the strength of selection for fitness and age-specific survival and fertility in a 19th century American population.Evolution. 2013; https://doi.org/10.1111/evo.12023Crossref Scopus (28) Google Scholar] and perhaps interfere with efforts to slow it down. However, developing realistic predictions won’t be easy considering that predicting evolution, even over a short term, is sometimes like trying to square the circle [20Morrissey M.B. Parker D.J. Korsten P. Pemberton J.M. Kruuk L.E.B. Wilson A.J. The prediction of adaptive evolution: empirical application of the secondary theorem of selection and comparison to the breeder's equation.Evolution. 2012; 66: 2399-2410Crossref PubMed Scopus (86) Google Scholar]. The Demographic Transition Influences Variance in Fitness and Selection on Height and BMI in Rural GambiaCourtiol et al.Current BiologyApril 25, 2013In BriefRecent human history is marked by demographic transitions characterized by declines in mortality and fertility [1]. By influencing the variance in those fitness components, demographic transitions can affect selection on other traits [2]. Parallel to changes in selection triggered by demography per se, relationships between fitness and anthropometric traits are also expected to change due to modification of the environment. Here we explore for the first time these two main evolutionary consequences of demographic transitions using a unique data set containing survival, fertility, and anthropometric data for thousands of women in rural Gambia from 1956–2010 [3]. Full-Text PDF Open Access" @default.
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• W2055750996 title "Human Evolution: New Playgrounds for Natural Selection" @default.
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