Browse by volume Browse by section Browse by topic Browse by conference

Section: Evolutionary Biology
Topic: Evolution, Population biology

Extrinsic mortality and senescence: a guide for the perplexed

de Vries, Charlotte1, 2, 3  ; Galipaud, Matthias3, 4; Kokko, Hanna3, 5, 6, 7 
1 Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, The Netherlands
2 Department of Biological and Environmental Science University of Jyväskylä, Jyväskylä, Finland
3 Department of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich, Switzerland
4 Swiss Data Science Center, Turnerstrasse 1, 8092, Zurich, Switzerland
5 Konrad Lorenz Institute of Ethology University of Veterinary Medicine Vienna, Austria
6 Faculty of Biological and Environmental Sciences University of Helsinki, Helsinki, Finland
7 Institute for Organismic and Molecular Evolution, Johannes Gutenberg-University Mainz, Mainz, Germany

10.24072/pcjournal.253 - Peer Community Journal, Volume 3 (2023), article no. e29.

Get full text PDF Peer reviewed and recommended by PCI

Do environments or species traits that lower the mortality of individuals create selection for delaying senescence? Reading the literature creates an impression that mathematically oriented biologists cannot agree on the validity of George Williams' prediction (who claimed 'yes'). The abundance of models and opinions may bewilder those that are new to the field. Here we provide heuristics as well as simple models that outline when the Williams prediction holds, why there is a ‘null model’ where extrinsic mortality does not change the evolution of senescence at all, and why it is also possible to expect the opposite of William’s prediction, where increased extrinsic mortality favours slower senescence. We hope to offer intuition by quantifying how much delaying the ‘placement’ of an offspring into the population reduces its expected contribution to the gene pool of the future. Our first example shows why sometimes increased extrinsic mortality has no effect (the null result), and why density dependence can change that. Thereafter, a model with ten different choices for population regulation shows that high extrinsic mortality favours fast life histories (Williams) if increasing density harms the production of juveniles or their chances to recruit into the population. If instead increasing density harms the survival of older individuals in a population, then high extrinsic mortality favours slow life histories (anti-Williams). We discuss the possibility that empirically found Williams-like patterns provide indirect evidence for population regulation operating via harming the production or fitness prospects of juveniles, as opposed to the survival of established breeders.

Published online:
DOI: 10.24072/pcjournal.253
Type: Research article
Keywords: Senescence, Life-History Evolution, Trade-Offs, Fast-slow life histories, Density dependence
Keywords: Senescence, Life-History Evolution, Trade-Offs, Fast-slow life histories, Density dependence
de Vries, Charlotte 1, 2, 3; Galipaud, Matthias 3, 4; Kokko, Hanna 3, 5, 6, 7

1 Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, The Netherlands
2 Department of Biological and Environmental Science University of Jyväskylä, Jyväskylä, Finland
3 Department of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich, Switzerland
4 Swiss Data Science Center, Turnerstrasse 1, 8092, Zurich, Switzerland
5 Konrad Lorenz Institute of Ethology University of Veterinary Medicine Vienna, Austria
6 Faculty of Biological and Environmental Sciences University of Helsinki, Helsinki, Finland
7 Institute for Organismic and Molecular Evolution, Johannes Gutenberg-University Mainz, Mainz, Germany
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights 
@article{10_24072_pcjournal_253,
     author = {de Vries, Charlotte and Galipaud, Matthias and Kokko, Hanna},
     title = {Extrinsic mortality and senescence: a guide for the perplexed},
     journal = {Peer Community Journal},
     eid = {e29},
     publisher = {Peer Community In},
     volume = {3},
     year = {2023},
     doi = {10.24072/pcjournal.253},
     url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.253/}
}
TY  - JOUR
AU  - de Vries, Charlotte
AU  - Galipaud, Matthias
AU  - Kokko, Hanna
TI  - Extrinsic mortality and senescence: a guide for the perplexed
JO  - Peer Community Journal
PY  - 2023
VL  - 3
PB  - Peer Community In
UR  - https://peercommunityjournal.org/articles/10.24072/pcjournal.253/
DO  - 10.24072/pcjournal.253
ID  - 10_24072_pcjournal_253
ER  - 
%0 Journal Article
%A de Vries, Charlotte
%A Galipaud, Matthias
%A Kokko, Hanna
%T Extrinsic mortality and senescence: a guide for the perplexed
%J Peer Community Journal
%D 2023
%V 3
%I Peer Community In
%U https://peercommunityjournal.org/articles/10.24072/pcjournal.253/
%R 10.24072/pcjournal.253
%F 10_24072_pcjournal_253
de Vries, Charlotte; Galipaud, Matthias; Kokko, Hanna. Extrinsic mortality and senescence: a guide for the perplexed. Peer Community Journal, Volume 3 (2023), article  no. e29. doi : 10.24072/pcjournal.253. https://peercommunityjournal.org/articles/10.24072/pcjournal.253/

Peer reviewed and recommended by PCI : 10.24072/pci.evolbiol.100626

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Abrams, P. A. The fitness costs of senescence: The evolutionary importance of events in early adult life, Evolutionary Ecology, Volume 5 (1991) no. 4, pp. 343-360 | DOI

[2] Abrams, P. A. Does Increased Mortality Favor the Evolution of More Rapid Senescence?, Evolution, Volume 47 (1993) no. 3 | DOI

[3] André, J.-B.; Rousset, F. Does extrinsic mortality accelerate the pace of life? A bare-bones approach, Evolution and Human Behavior, Volume 41 (2020) no. 6, pp. 486-492 | DOI

[4] Austad, S. N.; Fischer, K. E. Mammalian Aging, Metabolism, and Ecology: Evidence From the Bats and Marsupials, Journal of Gerontology, Volume 46 (1991) no. 2 | DOI

[5] Austad, S. N. Retarded senescence in an insular population of Virginia opossums ( Didelphis virginiana ), Journal of Zoology, Volume 229 (1993) no. 4, pp. 695-708 | DOI

[6] Baldini, R. The Importance of Population Growth and Regulation in Human Life History Evolution, PLOS ONE, Volume 10 (2015) no. 4 | DOI

[7] Belsky, J.; Steinberg, L.; Houts, R. M.; Halpern-Felsher, B. L. The development of reproductive strategy in females: Early maternal harshness → earlier menarche → increased sexual risk taking., Developmental Psychology, Volume 46 (2010) no. 1, pp. 120-128 | DOI

[8] Bird, D.; Freeman, J.; Robinson, E.; Maughan, G.; Finley, J. B.; Lambert, P. M.; Kelly, R. L. A first empirical analysis of population stability in North America using radiocarbon records, The Holocene, Volume 30 (2020) no. 9, pp. 1345-1359 | DOI

[9] Capdevila, P.; Stott, I.; Beger, M.; Salguero-Gómez, R. Towards a Comparative Framework of Demographic Resilience, Trends in Ecology and Evolution, Volume 35 (2020) no. 9, pp. 776-786 | DOI

[10] Carlson, S. M.; Hilborn, R.; Hendry, A. P.; Quinn, T. P. Predation by Bears Drives Senescence in Natural Populations of Salmon, PLoS ONE, Volume 2 (2007) no. 12 | DOI

Caswell, H. , 2001. Matrix Population Models: Construction, Analysis and Interpretation (2nd ed.). Sinauer Associates, Sunderland, Massachusetts

[12] Caswell, H. Extrinsic mortality and the evolution of senescence, Trends in Ecology and Evolution, Volume 22 (2007) no. 4, pp. 173-174 | DOI

[13] Caswell, H.; Salguero‐Gómez, R. Age, stage and senescence in plants, Journal of Ecology, Volume 101 (2013) no. 3, pp. 585-595 | DOI

[14] Caswell, H.; Shyu, E. Senescence, Selection Gradients and Mortality, The Evolution of Senescence in the Tree of Life, Cambridge University Press, 2017, pp. 56-82 | DOI

[15] Cayuela, H.; Lemaître, J.; Bonnaire, E.; Pichenot, J.; Schmidt, B. R. Population position along the fast–slow life‐history continuum predicts intraspecific variation in actuarial senescence, Journal of Animal Ecology, Volume 89 (2020) no. 4, pp. 1069-1079 | DOI

[16] Charlesworth, B. Evolutionary mechanisms of senescence, Genetica, Volume 91 (1993) no. 1-3, pp. 11-19 | DOI

[17] Charlesworth, B. Evolution in Age-Structured Populations, Cambridge University Press, 1994 | DOI

[18] Chen, H.-y.; Maklakov, A. A. Longer Life Span Evolves under High Rates of Condition-Dependent Mortality, Current Biology, Volume 22 (2012) no. 22, pp. 2140-2143 | DOI

[19] da Silva, J. Reports of the Death of Extrinsic Mortality Moulding Senescence Have Been Greatly Exaggerated, Evolutionary Biology, Volume 45 (2018) no. 2, pp. 140-143 | DOI

[20] da Silva, J. Williams’ Intuition about Extrinsic Mortality Was Correct, Trends in Ecology and Evolution, Volume 35 (2020) no. 5, pp. 378-379 | DOI

[21] Day, T.; Abrams, P. A. Density Dependence, Senescence, and Williams’ Hypothesis, Trends in Ecology and Evolution, Volume 35 (2020) no. 4, pp. 300-302 | DOI

[22] Dańko, M. J.; Burger, O.; Argasiński, K.; Kozłowski, J. Extrinsic Mortality Can Shape Life-History Traits, Including Senescence, Evolutionary Biology, Volume 45 (2018) no. 4, pp. 395-404 | DOI

[23] Dańko, M. J.; Burger, O.; Kozłowski, J. Density-dependence interacts with extrinsic mortality in shaping life histories, PLOS ONE, Volume 12 (2017) no. 10 | DOI

[24] Del Giudice, M. Rethinking the fast-slow continuum of individual differences, Evolution and Human Behavior, Volume 41 (2020) no. 6, pp. 536-549 | DOI

[25] Dinh, T.; Haselton, M. G.; Gangestad, S. W. “Fast” women? The effects of childhood environments on women's developmental timing, mating strategies, and reproductive outcomes, Evolution and Human Behavior, Volume 43 (2022) no. 2, pp. 133-146 | DOI

[26] Drury, K. L. S.; Dwyer, G. Combining Stochastic Models with Experiments to Understand the Dynamics of Monarch Butterfly Colonization, The American Naturalist, Volume 166 (2005) no. 6, pp. 731-750 | DOI

[27] Dudycha, J. L.; Tessier, A. J. Natural Genetic Variation of Life Span, Reproduction, and Juvenile Growth in Daphnia, Evolution, Volume 53 (1999) no. 6 | DOI

[28] Fernández-López de Pablo, J.; Gutiérrez-Roig, M.; Gómez-Puche, M.; McLaughlin, R.; Silva, F.; Lozano, S. Palaeodemographic modelling supports a population bottleneck during the Pleistocene-Holocene transition in Iberia, Nature Communications, Volume 10 (2019) no. 1 | DOI

[29] Frankenhuis, W. E.; Nettle, D. Current debates in human life history research, Evolution and Human Behavior, Volume 41 (2020) no. 6, pp. 469-473 | DOI

[30] Frankenhuis, W. E.; Nettle, D.; McNamara, J. M. Echoes of Early Life: Recent Insights From Mathematical Modeling, Child Development, Volume 89 (2018) no. 5, pp. 1504-1518 | DOI

[31] Freeman, J.; Robinson, E.; Beckman, N. G.; Bird, D.; Baggio, J. A.; Anderies, J. M. The global ecology of human population density and interpreting changes in paleo-population density, Journal of Archaeological Science, Volume 120 (2020) | DOI

[32] Gadgil, M.; Bossert, W. H. Life Historical Consequences of Natural Selection, The American Naturalist, Volume 104 (1970) no. 935, pp. 1-24 | DOI

[33] Gaillard, J.-M.; Lemaître, J.-F. The Williams' legacy: A critical reappraisal of his nine predictions about the evolution of senescence, Evolution, Volume 71 (2017) no. 12, pp. 2768-2785 | DOI

[34] Galipaud, M.; Kokko, H. Adaptation and plasticity in life-history theory: How to derive predictions., Evolution and Human Behavior, Volume 41 (2020) no. 6, pp. 493-501 | DOI

[35] Gavrilov, L. A.; Gavrilova, N. S. The Reliability Theory of Aging and Longevity, Journal of Theoretical Biology, Volume 213 (2001) no. 4, pp. 527-545 | DOI

[36] Gompertz, B. XXIV. On the nature of the function expressive of the law of human mortality, and on a new mode of determining the value of life contingencies. In a letter to Francis Baily, Esq. F. R. S. c, Philosophical Transactions of the Royal Society of London, Volume 115 (1825), pp. 513-583 | DOI

[37] Grant, J. W. A.; Weir, L. K.; Steingrímsson, S. Ó. Territory size decreases minimally with increasing food abundance in stream salmonids: Implications for population regulation, Journal of Animal Ecology, Volume 86 (2017) no. 6, pp. 1308-1316 | DOI

[38] Hamilton, M. J.; Milne, B. T.; Walker, R. S.; Burger, O.; Brown, J. H. The complex structure of hunter–gatherer social networks, Proceedings of the Royal Society B: Biological Sciences, Volume 274 (2007) no. 1622, pp. 2195-2203 | DOI

[39] Hamilton, M. J.; Burger, O.; DeLong, J. P.; Walker, R. S.; Moses, M. E.; Brown, J. H. Population stability, cooperation, and the invasibility of the human species, Proceedings of the National Academy of Sciences, Volume 106 (2009) no. 30, pp. 12255-12260 | DOI

[40] Hamilton, W. The moulding of senescence by natural selection, Journal of Theoretical Biology, Volume 12 (1966) no. 1, pp. 12-45 | DOI

[41] Healy, K.; Guillerme, T.; Finlay, S.; Kane, A.; Kelly, S. B. A.; McClean, D.; Kelly, D. J.; Donohue, I.; Jackson, A. L.; Cooper, N. Ecology and mode-of-life explain lifespan variation in birds and mammals, Proceedings of the Royal Society B: Biological Sciences, Volume 281 (2014) no. 1784 | DOI

[42] Holmes, D. J.; Austad, S. N. Fly Now, Die Later: Life-History Correlates of Gliding and Flying in Mammals, Journal of Mammalogy, Volume 75 (1994) no. 1, pp. 224-226 | DOI

[43] Jones, O. R.; Gaillard, J.-M.; Tuljapurkar, S.; Alho, J. S.; Armitage, K. B.; Becker, P. H.; Bize, P.; Brommer, J.; Charmantier, A.; Charpentier, M.; Clutton-Brock, T.; Dobson, F. S.; Festa-Bianchet, M.; Gustafsson, L.; Jensen, H.; Jones, C. G.; Lillandt, B.-G.; McCleery, R.; Merilä, J.; Neuhaus, P.; Nicoll, M. A. C.; Norris, K.; Oli, M. K.; Pemberton, J.; Pietiäinen, H.; Ringsby, T. H.; Roulin, A.; Saether, B.-E.; Setchell, J. M.; Sheldon, B. C.; Thompson, P. M.; Weimerskirch, H.; Jean Wickings, E.; Coulson, T. Senescence rates are determined by ranking on the fast-slow life-history continuum, Ecology Letters, Volume 11 (2008) no. 7, pp. 664-673 | DOI

[44] Jones, O. R.; Scheuerlein, A.; Salguero-Gómez, R.; Camarda, C. G.; Schaible, R.; Casper, B. B.; Dahlgren, J. P.; Ehrlén, J.; García, M. B.; Menges, E. S.; Quintana-Ascencio, P. F.; Caswell, H.; Baudisch, A.; Vaupel, J. W. Diversity of ageing across the tree of life, Nature, Volume 505 (2013) no. 7482, pp. 169-173 | DOI

[45] Kokko, H. The stagnation paradox: the ever-improving but (more or less) stationary population fitness, Proceedings of the Royal Society B: Biological Sciences, Volume 288 (2021) no. 1963 | DOI

[46] Kokko, H.; Hochberg, M. E. Towards cancer-aware life-history modelling, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 370 (2015) no. 1673 | DOI

[47] Koopman, J. J.; Wensink, M. J.; Rozing, M. P.; van Bodegom, D.; Westendorp, R. G. Intrinsic and extrinsic mortality reunited, Experimental Gerontology, Volume 67 (2015), pp. 48-53 | DOI

[48] Krüger, O.; Chakarov, N.; Nielsen, J. T.; Looft, V.; Grünkorn, T.; Struwe-Juhl, B.; Møller, A. P. Population regulation by habitat heterogeneity or individual adjustment?, Journal of Animal Ecology, Volume 81 (2011) no. 2, pp. 330-340 | DOI

[49] Laird, R. A.; Sherratt, T. N. The evolution of senescence through decelerating selection for system reliability, Journal of Evolutionary Biology, Volume 22 (2009) no. 5, pp. 974-982 | DOI

[50] Laird, R. A.; Sherratt, T. N. The evolution of senescence in multi-component systems, Biosystems, Volume 99 (2010) no. 2, pp. 130-139 | DOI

[51] Laird, R. A.; Sherratt, T. N. The economics of evolution: Henry Ford and the Model T, Oikos, Volume 119 (2010) no. 1, pp. 3-9 | DOI

[52] Lee, E. D.; Kempes, C. P.; West, G. B. Growth, death, and resource competition in sessile organisms, Proceedings of the National Academy of Sciences, Volume 118 (2021) no. 15 | DOI

[53] Lynch, R.; Lummaa, V.; Briga, M.; Chapman, S. N.; Loehr, J. Child volunteers in a women's paramilitary organization in World War II have accelerated reproductive schedules, Nature Communications, Volume 11 (2020) no. 1 | DOI

[54] López‐Sepulcre, A.; Kokko, H. Territorial Defense, Territory Size, and Population Regulation, The American Naturalist, Volume 166 (2005) no. 3, pp. 317-325 | DOI

[55] Makeham, W. M. On the Law of Mortality and the Construction of Annuity Tables, The Assurance Magazine and Journal of the Institute of Actuaries, Volume 8 (1860) no. 6, pp. 301-310 | DOI

[56] Maklakov, A. A.; Chapman, T. Evolution of ageing as a tangle of trade-offs: energy versus function, Proceedings of the Royal Society B: Biological Sciences, Volume 286 (2019) no. 1911 | DOI

[57] Medawar, P. An Unsolved Problem in Biology. , H.K. Lewis, London, 1952

[58] Missov, T. I.; Lenart, A. Gompertz–Makeham life expectancies: Expressions and applications, Theoretical Population Biology, Volume 90 (2013), pp. 29-35 | DOI

[59] Moorad, J.; Promislow, D.; Silvertown, J. George C. Williams’ Problematic Model of Selection and Senescence: Time to Move on, Trends in Ecology and Evolution, Volume 35 (2020) no. 4, pp. 303-305 | DOI

[60] Moorad, J.; Promislow, D.; Silvertown, J. Williams’ Intuition about Extrinsic Mortality Is Irrelevant, Trends in Ecology and Evolution, Volume 35 (2020) no. 5 | DOI

[61] Moorad, J.; Promislow, D.; Silvertown, J. Evolutionary Ecology of Senescence and a Reassessment of Williams’ ‘Extrinsic Mortality’ Hypothesis, Trends in Ecology and Evolution, Volume 34 (2019) no. 6, pp. 519-530 | DOI

[62] Mylius, S. D.; Diekmann, O. On Evolutionarily Stable Life Histories, Optimization and the Need to Be Specific about Density Dependence, Oikos, Volume 74 (1995) no. 2 | DOI

[63] Møller, A. P. Senescence in relation to latitude and migration in birds, Journal of Evolutionary Biology, Volume 20 (2007) no. 2, pp. 750-757 | DOI

[64] Nettle, D.; Frankenhuis, W. E.; Rickard, I. J. The evolution of predictive adaptive responses in human life history, Proceedings of the Royal Society B: Biological Sciences, Volume 280 (2013) no. 1766 | DOI

[65] Newton, I. Experiments On The Limitation Of Bird Numbers By Territorial Behaviour, Biological Reviews, Volume 67 (1992) no. 2, pp. 129-173 | DOI

[66] Promislow, D. E. L.; Harvey, P. H. Living fast and dying young: A comparative analysis of life‐history variation among mammals, Journal of Zoology, Volume 220 (1990) no. 3, pp. 417-437 | DOI

[67] Purchase, C. F.; Rooke, A. C.; Gaudry, M. J.; Treberg, J. R.; Mittell, E. A.; Morrissey, M. B.; Rennie, M. D. A synthesis of senescence predictions for indeterminate growth, and support from multiple tests in wild lake trout, Proceedings of the Royal Society B: Biological Sciences, Volume 289 (2022) no. 1966 | DOI

[68] Reznick, D. N.; Bryant, M. J.; Roff, D.; Ghalambor, C. K.; Ghalambor, D. E. Effect of extrinsic mortality on the evolution of senescence in guppies, Nature, Volume 431 (2004) no. 7012, pp. 1095-1099 | DOI

[69] Ricklefs, R. E. The evolution of senescence from a comparative perspective, Functional Ecology, Volume 22 (2008) no. 3, pp. 379-392 | DOI

[70] Roper, M.; Capdevila, P.; Salguero-Gómez, R. Senescence: why and where selection gradients might not decline with age, Proceedings of the Royal Society B: Biological Sciences, Volume 288 (2021) no. 1955 | DOI

[71] Sear, R. Do human ‘life history strategies’ exist?, Evolution and Human Behavior, Volume 41 (2020) no. 6, pp. 513-526 | DOI

[72] Sheehy-Skeffington, J. The effects of low socioeconomic status on decision-making processes, Current Opinion in Psychology, Volume 33 (2020), pp. 183-188 | DOI

[73] Stearns, S. C. Trade-Offs in Life-History Evolution, Functional Ecology, Volume 3 (1989) no. 3 | DOI

[74] Stearns, S. C.; Ackermann, M.; Doebeli, M.; Kaiser, M. Experimental evolution of aging, growth, and reproduction in fruitflies, Proceedings of the National Academy of Sciences, Volume 97 (2000) no. 7, pp. 3309-3313 | DOI

[75] Stearns, S. C.; Rodrigues, A. M. On the use of “life history theory” in evolutionary psychology, Evolution and Human Behavior, Volume 41 (2020) no. 6, pp. 474-485 | DOI

[76] Sæther, B.-E.; Engen, S.; Matthysen, E. Demographic Characteristics and Population Dynamical Patterns of Solitary Birds, Science, Volume 295 (2002) no. 5562, pp. 2070-2073 | DOI

[77] Sæther, B.-E.; Grøtan, V.; Engen, S.; Coulson, T.; Grant, P. R.; Visser, M. E.; Brommer, J. E.; Rosemary Grant, B.; Gustafsson, L.; Hatchwell, B. J.; Jerstad, K.; Karell, P.; Pietiäinen, H.; Roulin, A.; Røstad, O. W.; Weimerskirch, H. Demographic routes to variability and regulation in bird populations, Nature Communications, Volume 7 (2016) no. 1 | DOI

[78] Tatar, M.; Gray, D. W.; Carey, J. R. Altitudinal variation for senescence in Melanoplus grasshoppers, Oecologia, Volume 111 (1997) no. 3, pp. 357-364 | DOI

[79] Taylor, H. M.; Gourley, R. S.; Lawrence, C. E.; Kaplan, R. S. Natural selection of life history attributes: An analytical approach, Theoretical Population Biology, Volume 5 (1974) no. 1, pp. 104-122 | DOI

[80] Terzibasi Tozzini, E.; Dorn, A.; Ng’oma, E.; Polačik, M.; Blažek, R.; Reichwald, K.; Petzold, A.; Watters, B.; Reichard, M.; Cellerino, A. Parallel evolution of senescence in annual fishes in response to extrinsic mortality, BMC Evolutionary Biology, Volume 13 (2013) no. 1 | DOI

[81] Tuljapurkar, S. Population dynamics in variable environments, Lecture Notes in Biomathematics, 85, Springer Science Business Media, 2013

[82] Vaupel, J. W.; Baudisch, A.; Dölling, M.; A. Roach, D.; Gampe, J. The case for negative senescence, Theoretical Population Biology, Volume 65 (2004) no. 4, pp. 339-351 | DOI

[83] Wensink, M. J.; Caswell, H.; Baudisch, A. The Rarity of Survival to Old Age Does Not Drive the Evolution of Senescence, Evolutionary Biology, Volume 44 (2016) no. 1, pp. 5-10 | DOI

[84] Wilkinson, G. S.; Adams, D. M. Recurrent evolution of extreme longevity in bats, Biology Letters, Volume 15 (2019) no. 4 | DOI

[85] Williams, G. C. Pleiotropy, Natural Selection, and the Evolution of Senescence, Evolution, Volume 11 (1957) no. 4 | DOI

[86] Williams, P. D.; Day, T. Antagonistic Pleiotropy, Mortality Source Interactions, And The Evolutionary Theory Of Senescence, Evolution, Volume 57 (2003) no. 7, pp. 1478-1488 | DOI

[87] Woodley of Menie, M. A.; Luoto, S.; Peñaherrera-Aguirre, M.; Sarraf, M. A. Life History Is a Major Source of Adaptive Individual and Species Differences: a Critical Commentary on Zietsch and Sidari (2020), Evolutionary Psychological Science, Volume 7 (2021) no. 3, pp. 213-231 | DOI

[88] Zietsch, B. P.; Sidari, M. J. A critique of life history approaches to human trait covariation, Evolution and Human Behavior, Volume 41 (2020) no. 6, pp. 527-535 | DOI

Cited by Sources: