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Animal life history is shaped by the pace of life and the distribution of age-specific mortality and reproduction

Animal life history is shaped by the pace of life and the distribution of age-specific mortality and reproduction
Animal life history is shaped by the pace of life and the distribution of age-specific mortality and reproduction
Animals exhibit an extraordinary diversity of life history strategies. These realised combinations of survival, development, and reproduction are predicted to be constrained by physiological limitations and 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 both the fast-slow continuum and by a separate 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.


The turquoise killifish, Nothobranchius furzeri, can complete its lifecycle in just 14 days1. In contrast, the Greenland shark only becomes sexual mature after 156 years2. Despite their differences, the evolution of both these life histories is underpinned by the same evolutionary principal of maximising fitness through differing rates of survival, development, and reproduction3. As these species demonstrate, different combinations of traits associated with fitness, known as life history traits4, can successfully maintain viable populations over evolutionary time. The range of variation in life history traits and how they combine into life history strategies across the animal Kingdom is vast. Hexactinellid sponges can live for millennia5 while Gastrotrichs can complete their life cycle within days6. Pacific salmon (Oncorhynchus tshawytscha) release thousands of eggs in a single reproductive event7, while Laysan albatross (Phoebastria immutabilis) individuals are known to reproduce continuously for decades8. Understanding how variation in these traits combines into life history strategies, and in turn how these strategies relate to the range of forms, physiologies and ecologies found in the animal kingdom, is key to our understanding of questions ranging from the invasive potential of species9 to the evolution of senescence10.


Despite the diversity of life history strategies, not all are possible. Darwinian demons, hypothetical organisms which live forever and reproduce at infinite rates, do not exist due to limitations in resources11. The structure of life history strategies also reflects the environmental and physical constraints they evolve under. For example, to attain larger adult sizes individuals typically allocate resources towards development at the expense of reproductive output4. There are many such trade-offs that shape life history strategies12. The most well-understood of these results is the fast-slow continuum4,13 where the allocation of resources between survival, development, and reproduction results in a continuum of strategies ranging from a combination of fast development, short lifespans, and high reproductive rates, to combinations of slow development, longer lifespans, and low reproductive rates2. Additional axes of variation beyond the fast-slow continuum have also been described13-16. These typically relate to various moments of reproduction such as its annual intensity, duration, and its spread across the life course14.

Identifying these major axes of variation provides a framework which can aid in mapping how conservation management strategies17, degrees of invasiveness9 and diversity18 relate to different life history strategies. However, current patterns of animal life history strategies are either based on taxonomically restricted groups, typically Mammalia11 and Aves13,19, or do not account for the potential variation in life history traits that can be attributed to body size16. Hence our current understanding of patterns in life history strategies effectively misses the wider variation in life history traits observed across the animal kingdom. Here, we exploit the recent rapid expansion in taxonomic coverage of animal demographic data20 to incorporate age related measures of mortality and reproduction10, along with other life history traits (Figure 1), into a test of the universality of life history patterns from the level of populations to the scale of the animal evolutionary tree (Figure 2).
1217-1224
Healey, Kevin
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Ezard, Thomas
a143a893-07d0-4673-a2dd-cea2cd7e1374
Jones, Owen
f2c5b23b-40c4-4dbe-af40-f19bfd6bd2be
Salguero-Gomez, Roberto
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Buckley, Yvonne M.
3c773f90-cc7d-4db3-9a6a-1a3d79e000c3
Healey, Kevin
bf28b5b5-78b2-487e-8372-6c929209eb18
Ezard, Thomas
a143a893-07d0-4673-a2dd-cea2cd7e1374
Jones, Owen
f2c5b23b-40c4-4dbe-af40-f19bfd6bd2be
Salguero-Gomez, Roberto
d82c82b8-a1d4-47b5-ad62-8b2f5db217f7
Buckley, Yvonne M.
3c773f90-cc7d-4db3-9a6a-1a3d79e000c3

Healey, Kevin, Ezard, Thomas, Jones, Owen, Salguero-Gomez, Roberto and Buckley, Yvonne M. (2019) Animal life history is shaped by the pace of life and the distribution of age-specific mortality and reproduction. Nature Ecology and Evolution, 3 (8), 1217-1224. (doi:10.1038/s41559-019-0938-7).

Record type: Article

Abstract

Animals exhibit an extraordinary diversity of life history strategies. These realised combinations of survival, development, and reproduction are predicted to be constrained by physiological limitations and 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 both the fast-slow continuum and by a separate 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.


The turquoise killifish, Nothobranchius furzeri, can complete its lifecycle in just 14 days1. In contrast, the Greenland shark only becomes sexual mature after 156 years2. Despite their differences, the evolution of both these life histories is underpinned by the same evolutionary principal of maximising fitness through differing rates of survival, development, and reproduction3. As these species demonstrate, different combinations of traits associated with fitness, known as life history traits4, can successfully maintain viable populations over evolutionary time. The range of variation in life history traits and how they combine into life history strategies across the animal Kingdom is vast. Hexactinellid sponges can live for millennia5 while Gastrotrichs can complete their life cycle within days6. Pacific salmon (Oncorhynchus tshawytscha) release thousands of eggs in a single reproductive event7, while Laysan albatross (Phoebastria immutabilis) individuals are known to reproduce continuously for decades8. Understanding how variation in these traits combines into life history strategies, and in turn how these strategies relate to the range of forms, physiologies and ecologies found in the animal kingdom, is key to our understanding of questions ranging from the invasive potential of species9 to the evolution of senescence10.


Despite the diversity of life history strategies, not all are possible. Darwinian demons, hypothetical organisms which live forever and reproduce at infinite rates, do not exist due to limitations in resources11. The structure of life history strategies also reflects the environmental and physical constraints they evolve under. For example, to attain larger adult sizes individuals typically allocate resources towards development at the expense of reproductive output4. There are many such trade-offs that shape life history strategies12. The most well-understood of these results is the fast-slow continuum4,13 where the allocation of resources between survival, development, and reproduction results in a continuum of strategies ranging from a combination of fast development, short lifespans, and high reproductive rates, to combinations of slow development, longer lifespans, and low reproductive rates2. Additional axes of variation beyond the fast-slow continuum have also been described13-16. These typically relate to various moments of reproduction such as its annual intensity, duration, and its spread across the life course14.

Identifying these major axes of variation provides a framework which can aid in mapping how conservation management strategies17, degrees of invasiveness9 and diversity18 relate to different life history strategies. However, current patterns of animal life history strategies are either based on taxonomically restricted groups, typically Mammalia11 and Aves13,19, or do not account for the potential variation in life history traits that can be attributed to body size16. Hence our current understanding of patterns in life history strategies effectively misses the wider variation in life history traits observed across the animal kingdom. Here, we exploit the recent rapid expansion in taxonomic coverage of animal demographic data20 to incorporate age related measures of mortality and reproduction10, along with other life history traits (Figure 1), into a test of the universality of life history patterns from the level of populations to the scale of the animal evolutionary tree (Figure 2).

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Accepted/In Press date: 3 June 2019
e-pub ahead of print date: 8 July 2019
Published date: August 2019

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Local EPrints ID: 432258
URI: http://eprints.soton.ac.uk/id/eprint/432258
PURE UUID: a4715f7e-d82c-4a16-8599-26733b39956d
ORCID for Thomas Ezard: ORCID iD orcid.org/0000-0001-8305-6605

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Date deposited: 05 Jul 2019 16:30
Last modified: 07 Oct 2020 04:52

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Author: Kevin Healey
Author: Thomas Ezard ORCID iD
Author: Owen Jones
Author: Roberto Salguero-Gomez
Author: Yvonne M. Buckley

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