An empirical estimate of the generation time of mouse lemurs.
Madagascar
Microcebus murinus
molecular evolution
sex difference
survival
Journal
American journal of primatology
ISSN: 1098-2345
Titre abrégé: Am J Primatol
Pays: United States
ID NLM: 8108949
Informations de publication
Date de publication:
12 2019
12 2019
Historique:
received:
21
06
2019
revised:
25
09
2019
accepted:
08
10
2019
pubmed:
22
10
2019
medline:
20
6
2020
entrez:
22
10
2019
Statut:
ppublish
Résumé
The generation time of organisms drives the rate of change in populations and across evolutionary times. In long-lived species, generation time should also account for overlapping generations, and the average age of parents has been proposed as a best approximation under these conditions. This study uses this definition to estimate the generation time of a widely studied small primate, Microcebus murinus, based on parentage data generated for a free-living population over a 6-year period in northwestern Madagascar. The average age of parents was calculated separately for mothers and fathers of three different offspring cohorts that differed in the degree of demographic uncertainty. In addition, adult survival rates were calculated for males and females based on long-term capture data from the same population to estimate the possible upper limits of generation time. Adult survival was low with only 44% of adult females and 38% of adult males being recaptured at the beginning of their second breeding season. The average age of mothers was 1.56-1.91 years, pointing toward a 2-year female generation time due to the high proportion of 1-year old mothers in all three cohorts. Female generation time estimates were fairly stable across the three offspring cohorts. In contrast, the average age of fathers differed by more than 1 year from the first to the third offspring cohort (1.71-2.83 years) pointing toward a 3-year generation time, but also suggesting a higher degree of demographic uncertainty in the early years of the study. For future modeling purposes, we, therefore, propose to use the average, 2.5 years, of male and female values as new estimate for the generation time of mouse lemurs.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e23062Subventions
Organisme : Deutsche Forschungsgemeinschaft
ID : DFG Zi 345/12
Pays : International
Organisme : Bundesministerium für Bildung und Forschung
ID : 01LC1617A
Pays : International
Organisme : European Union ERA-NET BiodivERsA
ID : 2015-138
Pays : International
Organisme : Landesgraduiertenförderung Niedersachsen
Pays : International
Organisme : Cusanuswerk
Pays : International
Organisme : Deutscher Akademischer Austauschdienst
ID : HSP II
Pays : International
Organisme : Deutscher Akademischer Austauschdienst
ID : HSP III
Pays : International
Organisme : Deutscher Akademischer Austauschdienst
ID : TG
Pays : International
Informations de copyright
© 2019 The Authors. American Journal of Primatology published by Wiley Periodicals, Inc.
Références
Aleixo-Pais, I., Salmona, J., Sgarlata, G. M., Rakotonanahary, A., Sousa, A. P., Parreira, B., … Kun-Rodrigues, C. (2019). The genetic structure of a mouse lemur living in a fragmented habitat in Northern Madagascar. Conservation Genetics, 20(2), 229-243. https://doi.org/10.1007/s10592-018-1126-z
Allendorf, F. W., Luikart, G., & Aitken, S. N. (2013). Conservation and the genetics of populations. Chichester: John Wiley & Sons, Ltd.
Blair, C., Heckman, K. L., Russell, A. L., & Yoder, A. D. (2014). Multilocus coalescent analyses reveal the demographic history and speciation patterns of mouse lemur sister species. BMC Evolutionary Biology, 14(1), 57. https://doi.org/10.1186/1471-2148-14-57
Blanco, M. B., Rasoazanabary, E., & Godfrey, L. R. (2015). Unpredictable environments, opportunistic responses: Reproduction and population turnover in two wild mouse lemur species (Microcebus rufus and M. griseorufus) from eastern and western Madagascar. American Journal of Primatology, 77, 936-947. https://doi.org/10.1002/ajp.22423.
Bronikowski, A. M., Cords, M., Alberts, S. C., Altmann, J., Brockman, D. K., Fedigan, L. M., … Morris, W.F. (2016a). Female and male life tables for seven wild primate species. Scientific Data, 3, 160006. https://doi.org/10.1038/sdata.2016.6
Bronikowski, A. M., Cords, M., Alberts, S. C., Altmann, J., Brockman, D. K., Fedigan, L. M., … Morris, W. F. (2016b). Data from: Female and male life tables for seven wild primate species. Dryad Digital Repository, https://doi.org/10.5061/dryad.v28t5
Caswell, H. (2001). Matrix population models. Sunderland: Sinauer Press.
Chao, L., & Carr, D. E. (1993). The molecular clock and the relationship between population size and generation time. Evolution, 47(2), 688-690. https://doi.org/10.2307/2410082
Charlesworth, B. (1980). Evolution in age-structured populations. Cambridge: Cambridge University Press.
Craul, M., Chikhi, L., Sousa, V., Olivieri, G. L., Rabesandratana, A., Zimmermann, E., & Radespiel, U. (2009). Influence of forest fragmentation on an endangered large-bodied lemur in northwestern Madagascar. Biological Conservation, 142, 2862-2871. https://doi.org/10.1016/j.biocon.2009.05.026
Eberle, M., & Kappeler, P. M. (2004a). Sex in the dark: Determinants and consequences of mixed male mating tactics in Microcebus murinus, a small solitary nocturnal primate. Behavioral Ecology and Sociobiology, 57, 77-90. https://doi.org/10.1007/s00265-004-0826-1
Eberle, M., & Kappeler, P. M. (2004b). Selected polyandry: Female choice and inter-sexual conflict in a small nocturnal solitary primate (Microcebus murinus). Behavioral Ecology and Sociobiology, 57, 91-100. https://doi.org/10.1007/s00265-004-0823-4
Felsenstein, J. (1971). Inbreeding and variance effective numbers in populations with overlapping generations. Genetics, 68(4), 581-597.
Fenner, J. N. (2005). Cross-cultural estimation of the human generation interval for use in genetics-based population divergence studies. American Journal of Physical Anthropology, 128, 415-423. https://doi.org/10.1002/ajpa.20188
Goodnight, K. F., & Queller, D. C. (1999). Computer software for performing likelihood tests of pedigree relationship using genetic markers. Molecular Ecology, 8, 1231-1234.
Hämäläinen, A., Dammhahn, M., Aujard, F., Eberle, M., Hardy, I., Kappeler, P. M., … Perret, M. (2014). Senescence or selective disappearance? Age trajectories of body mass in wild and captive populations of a small-bodied primate. Proceedings of the Royal Society B: Biological Sciences, 281(1791), 20140830. https://doi.org/10.1098/rspb.2014.0830
Hawkins, M. T. R., Culligan, R. R., Frasier, C. L., Dikow, R. B., Hagenson, R., Lei, R., & Louis, E. E. (2018). Genome sequence and population declines in the critically endangered greater bamboo lemur (Prolemur simus) and implications for conservation. BMC Genomics, 19, 445. https://doi.org/10.1186/s12864-018-4841-4
Hill, W. G. (1979). A note on effective population size with overlapping generations. Genetics, 92(1), 317-322.
Kramer, M. (1988). Life-table (survival) analysis. In M. Kramer (Ed.), Clinical epidemiology and biostatistics (pp. 236-253). New York, NY: Springer.
Kraus, C., Eberle, M., & Kappeler, P. M. (2008). The costs of risky male behaviour: Sex differences in seasonal survival in a small sexually monomorphic primate. Proceedings of the Royal Society B: Biological Sciences, 275(1643), 1635-1644. https://doi.org/10.1098/rspb.2008.0200
Laird, C. D., McConaughy, B. L., & McCarthy, B. J. (1969). Rate of fixation of nucleotide substitutions in evolution. Nature, 224(5215), 149-154. https://doi.org/10.1038/224149a0
Lande, R., Engen, S., & Saether, B. E. (2003). Stochastic population dynamics in ecology and conservation. Oxford: Oxford University Press.
Langergraber, K. E., Prufer, K., Rowney, C., Boesch, C., Crockford, C., Fawcett, K., … Vigilant, L. (2012). Generation times in wild chimpanzees and gorillas suggest earlier divergence times in great ape and human evolution. Proceedings of the National Academy of Sciences of the United States of America, 109(39), 15716-15721. https://doi.org/10.1073/pnas.1211740109
Lawler, R. R. (2011). Demographic concepts and research pertaining to the study of wild primate populations. Yearbook of Physical Anthropology, 54, 63-85. https://doi.org/10.1002/ajpa.21611
Li, W. H., Ellsworth, D. L., Krushkal, J., Chang, B. H. J., & Hewett-Emmett, D. (1996). Rates of nucleotide substitution in primates and rodents and the generation time effect hypothesis. Molecular Phylogenetics and Evolution, 5(1), 182-187. https://doi.org/10.1006/mpev.1996.0012
Lutermann, H. (2001). Weibchenassoziationen und Fortpflanzungsstrategien beim Grauen Mausmaki (Microcebus murinus) in Nordwest-Madagaskar (unpublished doctoral dissertation). University of Hanover, Hanover.
Lutermann, H., Schmelting, B., Radespiel, U., Ehresmann, P., & Zimmermann, E. (2006). The role of survival for the evolution of female philopatry in a solitary forager, the grey mouse lemur (Microcebus murinus). Proceedings of the Royal Society B: Biological Sciences, 273(1600), 2527-2533. https://doi.org/10.1098/rspb.2006.3603
Marshall, T. C., Slate, J., Kruuk, L. E. B., & Pemberton, J. M. (1998). Statistical confidence for likelihood-based paternity inference in natural populations. Molecular Ecology, 7(5), 639-655. https://doi.org/10.1046/j.1365-294x.1998.00374.x
Martin, A. P., & Palumbi, S. R. (1993). Body size, metabolic rate, generation time, and the molecular clock. Proceedings of the National Academy of Sciences of the United States of America, 90(9), 4087-4091. https://doi.org/10.1073/pnas.90.9.4087
Nabholz, B., Glemin, S., & Galtier, N. (2008). Strong variations of mitochondrial mutation rate across mammals-The longevity hypothesis. Molecular Biology and Evolution, 25(1), 120-130. https://doi.org/10.1093/molbev/msm248
Olivieri, G., Zimmermann, E., Randrianambinina, B., Rasoloharijaona, S., Rakotondravony, D., Guschanski, K., & Radespiel, U. (2007). The ever-increasing diversity in mouse lemurs: Three new species in north and northwestern Madagascar. Molecular Phylogenetics and Evolution, 43(1), 309-327. https://doi.org/10.1016/j.ympev.2006.10.026
Olivieri, G. L., Sousa, V., Chikhi, L., & Radespiel, U. (2008).). From genetic diversity and structure to conservation: Genetic signature of recent population declines in three mouse lemur species (Microcebus spp.). Biological Conservation, 141(5), 1257-1271. https://doi.org/10.1016/j.biocon.2008.02.025
Perret, M. (1982). Influence du groupement social sur la reproduction de la femelle de Microcebus murinus (Miller, 1777). Zeitschrift für Tierpsychologie, 60(1), 47-65.
Radespiel, U., Lutermann, H., Schmelting, B., Bruford, M. W., & Zimmermann, E. (2003). Patterns and dynamics of sex-biased dispersal in a nocturnal primate, the grey mouse lemur, Microcebus murinus. Animal Behaviour, 65(4), 709-719. https://doi.org/10.1006/anbe.2003.2121
Radespiel, U., Sarikaya, Z., Zimmermann, E., & Bruford, M. W. (2001). Sociogenetic structure in a free-living nocturnal primate population: Sex-specific differences in the grey mouse lemur (Microcebus murinus). Behavioral Ecology and Sociobiology, 50(6), 493-502. https://doi.org/10.1007/s002650100402
Radespiel, U., & Zimmermann, E. (2003). The influence of familiarity, age, experience and female mate choice on pregnancies in captive grey mouse lemurs. Behaviour, 140, 301-318. https://doi.org/10.1163/156853903321826648
Rina Evasoa, M., Radespiel, U., Hasiniaina, A. F., Rasoloharijaona, S., Randrianambinina, B., Rakotondravony, R., & Zimmermann, E. (2018). Variation in reproduction of the smallest-bodied primate radiation, the mouse lemurs (Microcebus spp.): A synopsis. American Journal of Primatology, 80, 0275-2565. https://doi.org/10.1002/ajp.22874
Salmona, J., Heller, R., Quéméré, E., & Chikhi, L. (2017). Climate change and human colonization triggered habitat loss and fragmentation in Madagascar. Molecular Ecology, 26(19), 5203-5222. https://doi.org/10.1111/mec.14173
Schad, J., Ganzhorn, J. U., & Sommer, S. (2005). Parasite burden and constitution of major histocompatibility complex in the Malagasy mouse lemur, Microcebus murinus. Evolution, 59(2), 439-450.
Scheumann, M., Rabesandratana, A., & Zimmermann, E. (2007). Predation, communication, and cognition in lemurs. In S. L. Gursky, & K. A. I. Nekaris (Eds.), Primate anti-predator strategies (pp. 100-126). Oxford, UK: Springer.
Schmelting, B. (2001). Reproductive tactics in male grey mouse lemurs (Microcebus murinus, J.F. Miller 1777) in northwestern Madagascar (unpublished doctoral dissertation). University of Veterinary Medicine Hannover, Hannover.
Schmelting, B., Ehresmann, P., Lutermann, H., Randrianambinina, B., & Zimmermann, E. (2000). Reproduction of two sympatric mouse lemur species (Microcebus murinus and M. ravelobensis) in north-west Madagascar: First results of a long term study. In W. R. Lourenço, & S. M. Goodman (Eds.), Diversité et Endémisme à Madagascar (pp. 165-175). Paris: Société de Biogéographie.
Schmelting, B., Zimmermann, E., Berke, O., Bruford, M. W., & Radespiel, U. (2007). Experience-dependent recapture rates and reproductive success in male grey mouse lemurs (Microcebus murinus). American Journal of Physical Anthropology, 133, 743-752. https://doi.org/10.1002/ajpa.20566
Schneider, N., Chikhi, L., Currat, M., & Radespiel, U. (2010). Signals of recent spatial expansions in the grey mouse lemur (Microcebus murinus). BMC Evolutionary Biology, 10, 105. https://doi.org/10.1186/1471-2148-10-105
Sgarlata, G. M., Salmona, J., Aleixo-Pais, I., Rakotonanahary, A., Sousa, A. P., Kun-Rodrigues, C., … Chikhi, L. (2018). Genetic differentiation and demographic history of the northern rufous mouse lemur (Microcebus tavaratra) across a fragmented landscape in northern Madagascar. International Journal of Primatology, 39(1), 65-89. https://doi.org/10.1007/s10764-018-0015-0
Thomas, J. A., Welch, J. J., Lanfear, R., & Bromham, L. (2010). A generation time effect on the rate of molecular evolution in invertebrates. Molecular Biology and Evolution, 27(5), 1173-1180. https://doi.org/10.1093/molbev/msq009
Tsantes, C., & Stelper, M. E. (2009). Age at first reproduction explains rate variation in the strepsirrhine molecular clock. Proceedings of the National Academy of Sciences of the United States of America, 106(43), 18165-18170. https://doi.org/10.1073/pnas.0906686106
Webster, R. H., & Wilson Sayres, M. A. (2016). Genomic signatures of sex-biased demography: Progress and prospects. Current Opinion in Genetics & Development, 41, 62-71. https://doi.org/10.1016/j.gde.2016.08.002
Weir, J. T., & Schluter, D. (2008). Calibrating the avian molecular clock. Molecular Ecology, 17(10), 2321-2328. https://doi.org/10.1111/j.1365-294X.2008.03742.x
Weisrock, D. W., Rasoloarison, R. M., Fiorentino, I., Ralison, J. M., Goodman, S. M., Kappeler, P. M., & Yoder, A. D. (2010). Delimiting species without nuclear monophyly in Madagascar's mouse lemurs. PLoS One, 5(3):e9883. https://doi.org/10.1371/journal.pone.0009883
Wu, C. I., & Li, W. H. (1985). Evidence for higher rates of nucleotide substitution in rodents than in man. Proceedings of the National Academy of Sciences of the United States of America, 82, 1741-1745. https://doi.org/10.1073/pnas.82.6.1741
Xue, Y., Prado-Martinez, J., Sudmant, P. H., Narasimhan, V., Ayub, Q., Szpak, M., … Scally, A. (2015). Mountain gorilla genomes reveal the impact of long-term population decline and inbreeding. Science, 348(6231), 242-245. https://doi.org/10.1126/science.aaa3952
Yoder, A. D., Campbell, C. R., Blanco, M. B., Dos Reis, M., Ganzhorn, J. U., Goodman, S. M., … Weisrock, D. W. (2016). Geogenetic patterns in mouse lemurs (genus Microcebus) reveal the ghosts of Madagascar's forests past. Proceedings of the National Academy of Sciences of the United States of America, 113(29), 8049-8056. https://doi.org/10.1073/pnas.1601081113
Zimmermann, E., & Radespiel, U. (2015). Primate life histories. In W. Henke, & I. Tattersall (Eds.), Handbook of paleoanthropology (pp. 1527-1592). Berlin, Heidelberg: Springer. https://doi.org/10.1007/978-3-642-39979-4_38
Zohdy, S., Gerber, B. D., Tecot, S., Blanco, M. B., Winchester, J. M., Wright, P. C., & Jernvall, J. (2014). Teeth, sex, and testosterone: Aging in the world's smallest primate. PLoS One, 9(10):e109528. https://doi.org/10.1371/journal.pone.0109528