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Animal Life History Is Shaped by the Pace of Life and the Distribution of Age-Specific Mortality and Reproduction

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Animal Life History Is Shaped by the Pace of Life and the Distribution of Age-Specific Mortality and Reproduction ARTICLES https://doi.org/10.1038/s41559-019-0938-7 Animal life history is shaped by the pace of life and the distribution of age-specific mortality and reproduction Kevin Healy 1,2,3*, Thomas H. G. Ezard 4, Owen R. Jones5, Roberto Salguero-Gómez6,7,8,9,10 and Yvonne M. Buckley 2,10 Animals exhibit an extraordinary diversity of life history strategies. These realized combinations of survival, development and reproduction are predicted to be constrained by physiological limitations and by trade-offs in resource allocation. However, our understanding of these patterns is restricted to a few taxonomic groups. Using demographic data from 121 species, ranging from humans to sponges, we test whether such trade-offs universally shape animal life history strategies. We show that, after accounting for body mass and phylogenetic relatedness, 71% of the variation in animal life history strategies can be explained by life history traits associated with the fast–slow continuum (pace of life) and with a second axis defined by the distribution of age-specific mortality hazards and the spread of reproduction. While we found that life history strategies are associated with metabolic rate and ecological modes of life, surprisingly similar life history strategies can be found across the phylogenetic and physiological diversity of animals. he turquoise killifish, Nothobranchius furzeri, can complete its resources between survival, development and reproduction results life cycle in 14 d (ref. 1). In contrast, the Greenland shark only in a continuum of strategies ranging from a combination of fast Tbecomes sexually mature after 156 yr (ref. 2). Despite their dif- development, short lifespans and high reproductive rates, to combi- ferences, the evolution of both these life histories is underpinned nations of slow development, longer lifespans and low reproductive by the evolutionary principal of maximizing fitness through dif- rates2. Other axes of variation have also been described13–16. These fering rates of survival, development and reproduction3. As these typically relate to aspects of reproduction such as its annual inten- species demonstrate, different combinations of traits associated sity and duration, and its spread over the life course14. with fitness, known as life history traits4, can successfully maintain Identifying these axes of variation provides a framework that can viable populations over evolutionary time. The range of variation aid in mapping how conservation management strategies17, degrees in life history traits and how they combine into life history strate- of invasiveness9 and diversity18, relate to different life history strate- gies across the animal kingdom is vast. Hexactinellid sponges can gies. However, current patterns of animal life history strategies are live for millennia5 while Gastrotrichs can complete their life cycle described on the basis of taxonomically restricted groups, typically in days6. Pacific salmon (Oncorhynchus tshawytscha) release thou- Mammalia11 and Aves13,19, or do not account for the potential varia- sands of eggs in a single reproductive event7, while Laysan albatross tion in life history traits that can be attributed to body size16. Hence (Phoebastria immutabilis) are known to reproduce continuously our understanding of patterns in life history strategies effectively for decades8. Understanding how variation in these traits combines misses the wider variation in life history traits observed across the into life history strategies, and in turn how these strategies relate to animal kingdom. Here, we use the recent rapid expansion in taxo- the range of forms, physiologies and ecologies found in the animal nomic coverage of animal demographic data20 to incorporate age- kingdom, is key to understanding issues ranging from the invasive related measures of mortality and reproduction10, along with other potential of species9 to the evolution of senescence10. life history traits (Fig. 1), into a test of the universality of life history Despite the diversity of life history strategies, not all strategies patterns from the level of populations to the scale of the animal evo- are possible. Darwinian demons, hypothetical organisms that live lutionary tree (Fig. 2). forever and reproduce at infinite rates, do not exist due to limita- tions in resources11. Life history strategies also reflects the environ- Results mental and physical constraints they evolve under. For example, The variation in life history traits observed amongst animals is shown to attain larger adult sizes individuals typically allocate resources across six life history traits (Figs. 2 and 3). Variation in traits ranged towards development at the expense of reproductive output4. Many from generation times (T) of 2.4 to 53.2 yr in the eastern sand darter such trade-offs shape life history strategies12. The most well-under- (Ammocrypta pellucida) and the black-browed albatross (Thalassarche stood of these is the fast–slow continuum4,13 where the allocation of melanophris) to low variation in distributions of mortality risks found 1Ryan Institute, School of Natural Sciences, National University of Ireland Galway, Galway, Ireland. 2School of Natural Sciences, Zoology, Trinity College Dublin, Dublin, Ireland. 3School of Biology, University of St Andrews, St Andrews, UK. 4Ocean & Earth Science, National Oceanography Centre Southampton, University of Southampton Waterfront Campus, Southampton, UK. 5Department of Biology, University of Southern Denmark, Odense, Denmark. 6Department of Zoology, Oxford University, Oxford, UK. 7Department of Animal & Plant Sciences, University of Sheffield, Sheffield, UK. 8Centre for Biodiversity and Conservation Science, University of Queensland, St Lucia, Australia. 9Evolutionary Demography Laboratory, Max Plank Institute for Demographic Research, Rostock, Germany. 10These authors contributed equally: Roberto Salguero-Gómez, Yvonne M. Buckley. *e-mail: [email protected] NatURE ECOLogy & EVOLUTION | www.nature.com/natecolevol ARTICLES NATURE ECOLOGY & EVOLUTION Spread of Age at first G reproduction Lα reproduction Describes the range between Age at first reproduction is the iteroparous and semelparous on a age when individuals reach scale of 0 to 1 using the Gini index. sexual maturity. G = 1 G = 0 Lα Max Age Age Zero Distribution of Mean sexual σ mortality risk Ф reproductive rate We use the standard deviation Mean sexual reproductive of the age distribution of rate is the mean number death. of offspring per annum Life when the population was Life history stratagies with course at its stable state constant mortality throughout of a distribution. the life course will have low cohort values of σ. Life history stratagies where mortality is concentrated at particular parts of the life Ф course will have high values of σ. e Life expectancy Generation Lα post maturity T time Life expectancy post maturity is life The mean time between two expectancy of individuals from the consecutive generations. Calculated age of first reproduction (L ). as the time it takes for a population α to grow by a factor of its net reproductive rate (Ro) relative to its L growth rate ( ). e α λ Lα log (Ro) T = log (λ) Fig. 1 | Life history traits used in our analysis to describe the life history strategies of a given animal population. The circle represents the life course of a cohort from birth (0 yr) clockwise to death, with each different coloured concentric band describing the sequence and timing of life history events, quantified using the metrics described in the boxes. For more information on how these were calculated see Supplementary Methods. in humans (σ = 0.01) to the more highly variable mortality risks found As predicted by the fast–slow continuum, generation time, age at across the life course of the smooth Australian abalone (Haliotis first reproduction (L ) and life expectancy post-maturity ()e are all α La laevigata) (σ = 0.07, Fig. 2). Reproductive traits varied from mean positively correlated (Fig. 3). These three traits define one of the axes reproductive rates of 0.02 offspring a year in humans to 225,595 a of variation in life history strategies, which accounts for 46% of the year in northern pike (Esox lucius), with the distribution of reproduc- variation in the full analysis of the 121 species in our dataset (Fig. 3). tion ranging from semelparous species such as the Chinook salmon Along this axis, species range from short-lived early reproducers, (G = 0.83) to iteroparous species such as the Murray River turtle such as the Uinta ground squirrel (Urocitellus armatus) and the (Emydura macquarii, G = 0.18). greater prairie chicken (Tympanuchus cupido), to long-lived, slow- While life history traits vary greatly, the combinations of these maturing animals, such as the northern fulmar (Fulmarus glacialis) traits into life history strategies is reportedly relatively constrai and the violescent sea-whip (Paramuricea clavata). The association ned4,13,15,19,21–25. Here, we find that, after controlling for body size of these life history traits follows previous expectations, particularly and phylogenetic relatedness (Fig. 4, Supplementary Table 1 and in the case of La and T, which have been suggested as proxies of the Supplementary Fig. 1), animal life history strategies vary across two fast–slow continuum21. An axis relating to these traits is found in all axes of variation defined by: (1) traits associated with the fast–slow of our additional analyses of taxonomic groups (Mammalia, Aves, continuum and (2) the distribution
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