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Section: Ecology
Topic: Ecology, Evolution, Population biology

Evolutionary determinants of reproductive seasonality: A theoretical approach

Burtschell, Lugdiwine1, 2 ; Dezeure, Jules1, 3 ; Huchard, Elise1 ; Godelle, Bernard1
1 Institute of Evolutionary Sciences of Montpellier (ISEM), UMR 5554, Université de Montpellier, CNRS, IRD, EPHE, Montpellier, France
2 AgroParisTech, Paris, France
3 Centre d'Ecologie Fonctionnelle et Evolutive (CEFE), UMR 5175, Université de Montpellier, CNRS, IRD, EPHE, Montpellier, France

10.24072/pcjournal.286 - Peer Community Journal, Volume 3 (2023), article no. e56.

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Reproductive seasonality is a major adaptation to seasonal cycles and varies substantially among organisms. This variation, which was long thought to reflect a simple latitudinal gradient, remains poorly understood for many species, in part due to a lacunary theoretical framework. Because seasonal cycles are increasingly disrupted by climate change, a better understanding of the ecology of reproductive seasonality could generate important insights on how climate change may affect biodiversity. The goal of this study was to investigate the drivers of evolutionary transitions towards reproductive seasonality using a realistic agent-based optimisation model simulating the life cycle of a female yellow baboon, who typically breeds year-round. Specifically, we tested the influence of three ecological traits (environmental seasonality, productivity and unpredictability) and three life-history traits (daily reproductive energy expenditure, reproductive cycle length and infant extrinsic mortality) on the intensity of reproductive seasonality. To do so, we simulated diverse reproductive phenology strategies (from non-seasonal to highly seasonal), assessed which were optimal and computed, for the set of optimal strategies, the intensity of reproductive seasonality. We then induced variation in each trait of interest and examined how it affected the intensity of reproductive seasonality. We found substantial effects of all three environmental traits: high reproductive seasonality was favoured by high environmental seasonality, low environmental productivity and low unpredictability. It was further, and most strongly, favoured by high daily reproductive energy expenditure. In contrast, there was no effect of reproductive cycle length and infant extrinsic mortality. Our modelling approach successfully disentangled the effects of environmental seasonality, productivity and unpredictability on the intensity of reproductive seasonality, which likely all contribute to generate the well-known association between latitude and reproductive seasonality. Our results further highlight the critical importance of life history pace on the evolution of reproductive seasonality. Overall, this study contributes a powerful theoretical framework and modelling tool that may apply across the life-history space, as well as sheds new light on the emergence and maintenance of non-seasonal breeding in slow-living species, including humans.

Published online:
DOI: 10.24072/pcjournal.286
Type: Research article
Burtschell, Lugdiwine 1, 2; Dezeure, Jules 1, 3; Huchard, Elise 1; Godelle, Bernard 1

1 Institute of Evolutionary Sciences of Montpellier (ISEM), UMR 5554, Université de Montpellier, CNRS, IRD, EPHE, Montpellier, France
2 AgroParisTech, Paris, France
3 Centre d'Ecologie Fonctionnelle et Evolutive (CEFE), UMR 5175, Université de Montpellier, CNRS, IRD, EPHE, Montpellier, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights 
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Burtschell, Lugdiwine; Dezeure, Jules; Huchard, Elise; Godelle, Bernard. Evolutionary determinants of reproductive seasonality: A theoretical approach. Peer Community Journal, Volume 3 (2023), article  no. e56. doi : 10.24072/pcjournal.286. https://peercommunityjournal.org/articles/10.24072/pcjournal.286/

PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.ecology.100470

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] Alberts, S. C. Social influences on survival and reproduction: Insights from a long‐term study of wild baboons, Journal of Animal Ecology, Volume 88 (2019) no. 1, pp. 47-66 | DOI

[2] Altmann, J.; Alberts, S. Body mass and growth rates in a wild primate population, Oecologia, Volume 72 (1987) no. 1, pp. 15-20 | DOI

[3] Altmann, J.; Muruthi, P. Differences in daily life between semiprovisioned and wild-feeding baboons, American Journal of Primatology, Volume 15 (1988) no. 3, pp. 213-221 | DOI

[4] Altmann, S. A. Foraging for survival: Yearling baboons in Africa, University of Chicago Press, Chicago, 1998

[5] Amboseli Baboon Research Project Available from: https://amboselibaboons.nd.edu/video/., ABRP GPS tracking of baboon social groups, 2015 (https://amboselibaboons.nd.edu/video/)

[6] Baniel, A.; Cowlishaw, G.; Huchard, E. Context dependence of female reproductive competition in wild chacma baboons, Animal Behaviour, Volume 139 (2018), pp. 37-49 | DOI

[7] Bielby, J.; Mace, G. M.; Bininda‐Emonds, O. R. P.; Cardillo, M.; Gittleman, J. L.; Jones, K. E.; Orme, C. D. L.; Purvis, A. The fast‐slow continuum in mammalian life history: An empirical reevaluation, The American Naturalist, Volume 169 (2007) no. 6, pp. 748-757 | DOI

[8] Botero, C. A.; Dor, R.; McCain, C. M.; Safran, R. J. Environmental harshness is positively correlated with intraspecific divergence in mammals and birds, Molecular Ecology, Volume 23 (2014) no. 2, pp. 259-268 | DOI

[9] Bradshaw, W. E.; Holzapfel, C. M. Evolution of animal photoperiodism, Annual Review of Ecology, Evolution, and Systematics, Volume 38 (2007) no. 1, pp. 1-25 | DOI

[10] Brockman, D. K.; van Schaik, C. P. Seasonality and reproductive function, Seasonality in Primates, Cambridge University Press, 2005, pp. 269-306 | DOI

[11] Bronson, F. H. Mammalian reproduction: An ecological perspective, Biology of Reproduction, Volume 32 (1985) no. 1, pp. 1-26 | DOI

[12] Bronson, F. H. Seasonal variation in human reproduction: Environmental factors, The Quarterly Review of Biology, Volume 70 (1995) no. 2, pp. 141-164 | DOI

[13] Bronson, F. H. Climate change and seasonal reproduction in mammals, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 364 (2009) no. 1534, pp. 3331-3340 | DOI

[14] Brown, G. P.; Shine, R. Why do most tropical animals reproduce seasonally? Testing hypotheses on an Australian snake, Ecology, Volume 87 (2006) no. 1, pp. 133-143 | DOI

[15] Buchan, J. C.; Alberts, S. C.; Silk, J. B.; Altmann, J. True paternal care in a multi-male primate society, Nature, Volume 425 (2003) no. 6954, pp. 179-181 | DOI

[16] Burtschell, L. Evolutionary determinants of reproductive seasonality: a theoretical approach [Dataset], Zenodo, 2023 | DOI

[17] Campos, F. A.; Morris, W. F.; Alberts, S. C.; Altmann, J.; Brockman, D. K.; Cords, M.; Pusey, A.; Stoinski, T. S.; Strier, K. B.; Fedigan, L. M. Does climate variability influence the demography of wild primates? Evidence from long-term life-history data in seven species, Global Change Biology, Volume 23 (2017) no. 11, pp. 4907-4921 | DOI

[18] Charpentier, M. J. E.; Tung, J.; Altmann, J.; Alberts, S. C. Age at maturity in wild baboons: genetic, environmental and demographic influences, Molecular Ecology, Volume 17 (2008) no. 8, pp. 2026-2040 | DOI

[19] Chen, D.; Cane, M. A.; Kaplan, A.; Zebiak, S. E.; Huang, D. Predictability of El Niño over the past 148 years, Nature, Volume 428 (2004) no. 6984, pp. 733-736 | DOI

[20] Clauss, M.; Zerbe, P.; Bingaman Lackey, L.; Codron, D.; Müller, D. W. H. Basic considerations on seasonal breeding in mammals including their testing by comparing natural habitats and zoos, Mammalian Biology, Volume 101 (2021) no. 4, pp. 373-386 | DOI

[21] Colwell, R. K. Predictability, constancy, and contingency of periodic phenomena, Ecology, Volume 55 (1974) no. 5, pp. 1148-1153 | DOI

[22] Conover, D. O. Seasonality and the scheduling of life history at different latitudes, Journal of Fish Biology, Volume 41 (1992) no. sb, pp. 161-178 | DOI

[23] Coulson, T. When does seasonal reproduction evolve?, Peer Community in Ecology no. 100470 | DOI

[24] Dezeure, J.; Baniel, A.; Carter, A.; Cowlishaw, G.; Godelle, B.; Huchard, E. Birth timing generates reproductive trade-offs in a non-seasonal breeding primate, Proceedings of the Royal Society B: Biological Sciences, Volume 288 (2021) no. 1950 | DOI

[25] Dezeure, J.; Burtschell, L.; Baniel, A.; Carter, A. J.; Godelle, B.; Cowlishaw, G.; Huchard, E. Evolutionary determinants of nonseasonal breeding in wild Chacma Baboons, The American Naturalist, Volume 201 (2023) no. 1, pp. 106-124 | DOI

[26] Dezeure, J.; Charpentier, M. J.; Huchard, E. Fitness effects of seasonal birth timing in a long-lived social primate living in the equatorial forest, Animal Behaviour, Volume 185 (2022), pp. 113-126 | DOI

[27] Di Bitetti, M. S.; Janson, C. H. When will the stork arrive? Patterns of birth seasonality in neotropical primates, American Journal of Primatology, Volume 50 (2000) no. 2, pp. 109-130 | DOI

[28] Didan, K. MOD13Q1 MODIS/Terra Vegetation Indices 16-Day L3 Global 250m SIN Grid V006, 2015 (https://doi.org/10.5067/MODIS/MOD13Q1.006)

[29] Dufour, D.; Sauther, M. Comparative and evolutionary dimensions of the energetics of human pregnancy and lactation, American Journal of Human Biology, Volume 14 (2002) no. 5, pp. 584-602 | DOI

[30] Easterling, D. R.; Meehl, G. A.; Parmesan, C.; Changnon, S. A.; Karl, T. R.; Mearns, L. O. Climate extremes: Observations, modeling, and impacts, Science, Volume 289 (2000) no. 5487, pp. 2068-2074 | DOI

[31] Eddelbuettel, D.; François, R. Rcpp: Seamless R and C++ integration, Journal of Statistical Software, Volume 40 (2011) no. 8 | DOI

[32] English, A. K.; Chauvenet, A. L. M.; Safi, K.; Pettorelli, N. Reassessing the determinants of breeding synchrony in ungulates, PLoS ONE, Volume 7 (2012) no. 7 | DOI

[33] Gesquiere, L. R.; Altmann, J.; Archie, E. A.; Alberts, S. C. Interbirth intervals in wild baboons: Environmental predictors and hormonal correlates, American Journal of Physical Anthropology, Volume 166 (2018) no. 1, pp. 107-126 | DOI

[34] Gesquiere, L. R.; Khan, M.; Shek, L.; Wango, T. L.; Wango, E. O.; Alberts, S. C.; Altmann, J. Coping with a challenging environment: Effects of seasonal variability and reproductive status on glucocorticoid concentrations of female baboons (Papio cynocephalus), Hormones and Behavior, Volume 54 (2008) no. 3, pp. 410-416 | DOI

[35] Grimm, V.; Berger, U.; DeAngelis, D. L.; Polhill, J. G.; Giske, J.; Railsback, S. F. The ODD protocol: A review and first update, Ecological Modelling, Volume 221 (2010) no. 23, pp. 2760-2768 | DOI

[36] Gruyer, N.; Gauthier, G.; Berteaux, D. Demography of two lemming species on Bylot Island, Nunavut, Canada, Polar Biology, Volume 33 (2010) no. 6, pp. 725-736 | DOI

[37] Heldstab, S. A. Habitat characteristics and life history explain reproductive seasonality in lagomorphs, Mammalian Biology, Volume 101 (2021a) no. 6, pp. 739-757 | DOI

[38] Heldstab, S. A. Latitude, life history and sexual size dimorphism correlate with reproductive seasonality in rodents, Mammal Review, Volume 51 (2021b) no. 2, pp. 256-271 | DOI

[39] Heldstab, S. A.; Müller, D. W. H.; Graber, S. M.; Bingaman Lackey, L.; Rensch, E.; Hatt, J.-M.; Zerbe, P.; Clauss, M. Geographical origin, delayed implantation, and induced ovulation explain reproductive seasonality in the carnivora, Journal of Biological Rhythms, Volume 33 (2018) no. 4, pp. 402-419 | DOI

[40] Heldstab, S. A.; van Schaik, C. P.; Müller, D. W. H.; Rensch, E.; Lackey, L. B.; Zerbe, P.; Hatt, J.; Clauss, M.; Matsuda, I. Reproductive seasonality in primates: Patterns, concepts and unsolved questions, Biological Reviews, Volume 96 (2021) no. 1, pp. 66-88 | DOI

[41] Hongo, S.; Nakashima, Y.; Akomo-Okoue, E. F.; Mindonga-Nguelet, F. L. Female reproductive seasonality and male influxes in wild mandrills (Mandrillus sphinx), International Journal of Primatology, Volume 37 (2016) no. 3, pp. 416-437 | DOI

[42] Ims, R. A. The ecology and evolution of reproductive synchrony, Trends in Ecology & Evolution, Volume 5 (1990) no. 5, pp. 135-140 | DOI

[43] Janson, C.; Verdolin, J. Seasonality of primate births in relation to climate, Seasonality in Primates: Studies of living and extinct human and non-human primates, Cambridge University Press, 2005, pp. 307-350 | DOI

[44] Jones, J. H. Primates and the evolution of long, slow life histories, Current Biology, Volume 21 (2011) no. 18 | DOI

[45] Keller, B. J.; Bleisch, A. D.; Millspaugh, J. J.; Lehman, C. P.; Kragel, J. J.; Hansen, L. P.; Sumners, J.; Rumble, M. A.; Brundige, G. C. Extended duration of parturition season in North American elk (Cervus elaphus), The American Midland Naturalist, Volume 173 (2015) no. 1, pp. 162-167 | DOI

[46] Kristensen, N. P.; Johansson, J.; Ripa, J.; Jonzén, N. Phenology of two interdependent traits in migratory birds in response to climate change, Proceedings of the Royal Society B: Biological Sciences, Volume 282 (2015) no. 1807 | DOI

[47] Loe, L. E.; Bonenfant, C.; Mysterud, A.; Gaillard, J.-M.; Langvatn, R.; Klein, F.; Calenge, C.; Ergon, T.; Pettorelli, N.; Stenseth, N. C. Climate predictability and breeding phenology in red deer: Timing and synchrony of rutting and calving in Norway and France, Journal of Animal Ecology, Volume 74 (2005) no. 4, pp. 579-588 | DOI

[48] Lukas, D.; Huchard, E. The evolution of infanticide by males in mammalian societies, Science, Volume 346 (2014) no. 6211, pp. 841-844 | DOI

[49] Lund, U.; Agostinelli, C.; Agostinelli, M. C. Package ‘circular’, Repository CRAN, 2017, pp. 1-142 (https://cran.r-project.org/web/packages/circular/circular.pdf)

[50] Macfarlan, S. J.; Schacht, R.; Bourland, I.; Kapp, S.; Glad, T.; Lewis, L.; Claflin, S.; Darmiento, N.; Clegg, T.; Thorpe, C.; Peppelar, T.; Hall, R. G.; Nguyen, B.; Davis, C. A.; Santiago, M.; Henrickson, C. NDVI predicts birth seasonality in historical Baja California Sur, Mexico: Adaptive responses to arid ecosystems and the North American monsoon, Biodemography and Social Biology, Volume 66 (2021) no. 2, pp. 145-155 | DOI

[51] Markham, A. C.; Guttal, V.; Alberts, S. C.; Altmann, J. When good neighbors don't need fences: Temporal landscape partitioning among baboon social groups, Behavioral Ecology and Sociobiology, Volume 67 (2013) no. 6, pp. 875-884 | DOI

[52] McGraw, J. B.; Caswell, H. Estimation of individual fitness from life-history data, The American Naturalist, Volume 147 (1996) no. 1, pp. 47-64 | DOI

[53] McLean, E. M.; Archie, E. A.; Alberts, S. C. Lifetime fitness in wild female baboons: Trade-offs and individual heterogeneity in quality, The American Naturalist, Volume 194 (2019) no. 6, pp. 745-759 | DOI

[54] Ogutu, J. O.; Piepho, H.-P.; Dublin, H. T. Reproductive seasonality in African ungulates in relation to rainfall, Wildlife Research, Volume 41 (2014) no. 4 | DOI

[55] Palombit, R. A. Male infanticide in wild savanna baboons: Adaptive significance and intraspecific variation, Sexual selection and reproductive competition in primates: New perspectives and directions, Volume 3 (2003), pp. 367-411 (https://citeseerx.ist.psu.edu/document?repid=rep1&type=pdf&doi=3100fb0b95694dcee698b45fe0204e4b99696bea)

[56] Petersdorf, M.; Weyher, A. H.; Kamilar, J. M.; Dubuc, C.; Higham, J. P. Sexual selection in the Kinda baboon, Journal of Human Evolution, Volume 135 (2019) | DOI

[57] Pettorelli, N.; Vik, J. O.; Mysterud, A.; Gaillard, J.-M.; Tucker, C. J.; Stenseth, N. C. Using the satellite-derived NDVI to assess ecological responses to environmental change, Trends in Ecology & Evolution, Volume 20 (2005) no. 9, pp. 503-510 | DOI

[58] Post, D. G. Feeding behavior of yellow baboons (Papio cynocephalusin) the Amboseli National Park, Kenya, International Journal of Primatology, Volume 3 (1982) no. 4, pp. 403-430 | DOI

[59] R: A language and environment for statistical computing, R Core Team, 2020 (http://www.r-project.org/index.html)

[60] Riedman, M. L.; Estes, J. A.; Staedler, M. M.; Giles, A. A.; Carlson, D. R. Breeding patterns and reproductive success of California sea otters, The Journal of Wildlife Management, Volume 58 (1994) no. 3 | DOI

[61] Samuels, A.; Altmann, J. Baboons of the amboseli basin: Demographic stability and change, International Journal of Primatology, Volume 12 (1991) no. 1, pp. 1-19 | DOI

[62] Setchell, J. M.; Lee, P. C.; Wickings, E. J.; Dixson, A. F. Growth and ontogeny of sexual size dimorphism in the mandrill (Mandrillus sphinx), American Journal of Physical Anthropology, Volume 115 (2001) no. 4, pp. 349-360 | DOI

[63] Sinclair, A. R. E.; Mduma, S. A. R.; Arcese, P. What determines phenology and synchrony of ungulate breeding in Serengeti?, Ecology, Volume 81 (2000) no. 8 | DOI

[64] Stearns, S. C. Trade-Offs in life-history evolution, Functional Ecology, Volume 3 (1989) no. 3 | DOI

[65] Stephens, P. A.; Houston, A. I.; Harding, K. C.; Boyd, I. L.; McNamara, J. M. Capital and income breeding: The role of food supply, Ecology, Volume 95 (2014) no. 4, pp. 882-896 | DOI

[66] Sun, Z.; Parvinen, K.; Heino, M.; Metz, J. A. J.; de Roos, A. M.; Dieckmann, U. Evolution of reproduction periods in seasonal environments, The American Naturalist, Volume 196 (2020) no. 4 | DOI

[67] Thackeray, S. J.; Henrys, P. A.; Hemming, D.; Bell, J. R.; Botham, M. S.; Burthe, S.; Helaouet, P.; Johns, D. G.; Jones, I. D.; Leech, D. I.; Mackay, E. B.; Massimino, D.; Atkinson, S.; Bacon, P. J.; Brereton, T. M.; Carvalho, L.; Clutton-Brock, T. H.; Duck, C.; Edwards, M.; Elliott, J. M.; Hall, S. J. G.; Harrington, R.; Pearce-Higgins, J. W.; Høye, T. T.; Kruuk, L. E. B.; Pemberton, J. M.; Sparks, T. H.; Thompson, P. M.; White, I.; Winfield, I. J.; Wanless, S. Phenological sensitivity to climate across taxa and trophic levels, Nature, Volume 535 (2016) no. 7611, pp. 241-245 | DOI

[68] Thel, L.; Chamaillé‐Jammes, S.; Bonenfant, C. How to describe and measure phenology? An investigation on the diversity of metrics using phenology of births in large herbivores, Oikos, Volume 2022 (2022) no. 4 | DOI

[69] Tökölyi, J.; McNamara, J. M.; Houston, A. I.; Barta, Z. Timing of avian reproduction in unpredictable environments, Evolutionary Ecology, Volume 26 (2012) no. 1, pp. 25-42 | DOI

[70] van Noordwijk, M. A.; Willems, E. P.; Utami Atmoko, S. S.; Kuzawa, C. W.; van Schaik, C. P. Multi-year lactation and its consequences in Bornean orangutans (Pongo pygmaeus wurmbii), Behavioral Ecology and Sociobiology, Volume 67 (2013) no. 5, pp. 805-814 | DOI

[71] van Schaik, C. P.; Brockman, D. K. Seasonality in primate ecology, reproduction, and life history: An overview, Seasonality in Primates: Studies of living and extinct human and non-human primates, Cambridge University Press, 2005, pp. 3-20 | DOI

[72] Vatka, E.; Rytkönen, S.; Orell, M. Does the temporal mismatch hypothesis match in boreal populations?, Oecologia, Volume 176 (2014) no. 2, pp. 595-605 | DOI

[73] Walton, B. J.; Findlay, L. J.; Hill, R. A. Insights into short‐ and long‐term crop‐foraging strategies in a chacma baboon (Papio ursinus) from GPS and accelerometer data, Ecology and Evolution, Volume 11 (2021) no. 2, pp. 990-1001 | DOI

[74] Wells, J. C.; Stock, J. T. The biology of the colonizing ape, American Journal of Physical Anthropology, Volume 134 (2007) no. S45, pp. 191-222 | DOI

[75] Zerbe, P.; Clauss, M.; Codron, D.; Bingaman Lackey, L.; Rensch, E.; Streich, J. W.; Hatt, J.-M.; Müller, D. W. H. Reproductive seasonality in captive wild ruminants: Implications for biogeographical adaptation, photoperiodic control, and life history, Biological Reviews, Volume 87 (2012) no. 4, pp. 965-990 | DOI

[76] Zinner, D.; Krebs, E.; Schrod, A.; Kaumanns, W. Early sexual maturity in male hamadryas baboons (Papio hamadryas hamadryas) and its reproductive implications, American Journal of Physical Anthropology, Volume 129 (2006) no. 4, pp. 584-590 | DOI

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