Meta-analysis shows no consistent evidence for senescence in ejaculate traits across animals

Krish Sanghvi; Regina Vega-Trejo; Shinichi Nakagawa; Samuel J. L. Gascoigne; Sheri L. Johnson; Roberto Salguero-Gómez; Tommaso Pizzari; Irem Sepil

doi:10.1038/s41467-024-44768-4

Meta-analysis shows no consistent evidence for senescence in ejaculate traits across animals

Krish Sanghvi
, Regina Vega-Trejo
, Shinichi Nakagawa
, Samuel J. L. Gascoigne
, Sheri L. Johnson
, Roberto Salguero-Gómez
, Tommaso Pizzari
, Irem Sepil

Research output: Contribution to journal › Article › peer-review

10 Citations (Scopus)

4 Downloads (Pure)

Abstract

Male reproductive traits such as ejaculate size and quality, are expected to decline with advancing age due to senescence. It is however unclear whether this expectation is upheld across taxa. We perform a meta-analysis on 379 studies, to quantify the effects of advancing male age on ejaculate traits across 157 species of non-human animals. Contrary to predictions, we find no consistent pattern of age-dependent changes in ejaculate traits. This result partly reflects methodological limitations, such as studies sampling a low proportion of adult lifespan, or the inability of meta-analytical approaches to document non-linear ageing trajectories of ejaculate traits; which could potentially lead to an underestimation of senescence. Yet, we find taxon-specific differences in patterns of ejaculate senescence. For instance, older males produce less motile and slower sperm in ray-finned fishes, but larger ejaculates in insects, compared to younger males. Notably, lab rodents show senescence in most ejaculate traits measured. Our study challenges the notion of universal reproductive senescence, highlighting the need for controlled methodologies and a more nuanced understanding of reproductive senescence, cognisant of taxon-specific biology, experimental design, selection pressures, and life-history.

Original language	English
Article number	558
Number of pages	13
Journal	Nature Communications
Volume	15
Early online date	16 Jan 2024
DOIs	https://doi.org/10.1038/s41467-024-44768-4
Publication status	Published - 2024
Externally published	Yes

Bibliographical note

We are extremely grateful to all the researchers who provided us with unpublished/missing data and life tables for various species, without whom our meta-analysis would not be possible: Abdallah Assiri, Adolfo Cordero, Adrienne Crosier, Alberto Velando, Alfonso Bolarin, Aline Malawey, Alistair Senior, Anders Pape Moller, Anil Kumar, Antje Girndt, Ashley Watt, Asim Orem, Bradley Metz, Bryan Neff, Budhan Pukazhenthi, Charles Fox, Chris Friesen, Chris Weldon, Christine Miller, Christophe Bressac, Claudia Fricke, Claudio Maia, Claus Wedekind, Clelia Gasparini, Clint McDonald, Craig Packer, Daniel Sasson, Davnah Payne, Diana Perez Staples Folger, Martha Reyez Hernandez, Distl Ottmar, Elena Zambrano, Emily “Becky” Cramer, Emily Duval, Erin MacCartney, Felipe Martinez, Fumio Hayashi, Gabriele Sorci, Gerard Wilkinson, Gerlind Lehmann, Gregor Majdic, Hasan Sevgili, Heriberto Martinez, Ilie Racotta, Ioannis Tsakmakidis, Jan Lifjeld, Jane Hurst, Janice Bailey, Maurice Clotilde, Jesus Dorado, Jurgen Heinze, Karen Lockyear, Karolina Stasiak, Katarzyna Kotarska, Kathrin Langen, Klaus Reinhardt, Leandro Miranda, Leslie Curren, Linda Penfold, Maira Brito, Malgorzata Kruczek, Manasi Kanuga, Marion Mehlis, Mark Elgar, Martin Brinkworth, Martin Schulze, Maud Bonato, Megan Head, Melissah Rowe, Michael Greenfield, Michael Ritchie, Michele Di Iorio, Michelle Helinski, Milos Krist, Moira O’Bryan, Muhammed Ines Inanc, Naomi Pierce, Nicolaia Iaffaldano, Nikos Papadopolous, Nikron Thongtip, Nils Cordes, Nucharin Songsasen, Megan Brown, Pablo Bermejo Alvares, Paco Garcia Gonzales, Panos Milonas, Patricia Diogo, Paul Joseph, Philip Downing, Priscilla Ramos, Rakesh Seth, Stuart Reynolds, Rebecca Dean, Sachiko Koyama, Satoshi Hiroyoshi, Silvia Cerolini, Sina Metzler, Stanislaw Kondrack, Stefan Luepold, Steven Ramm, Stuart Meyers, Theo Bakker, Tobias Kehl, Triin Hallap, Ulrike Luderer, Upama Aich, Wael Farag, Wei Shi, Wen Liao, Xiaoxu Li, Yasaman Alavi, Yih Fwu Lin, and Yingmei Zhang. We are also thankful to Milan Vrtilek, Rose O’Dea, Kevin Foster, Ana Silva, and Ellie Bath for their helpful comments and suggestions, as well as members of the Biology of Sperm Conference, 2023, for constructive criticism. Finally, we thank Neil Gemmell who supported preliminary meta-analytic investigations conducted by SJ and SN.

Data Availability Statement

Data availability
The data generated in this study have been deposited in the Open Science Framework database (https://osf.io/dk8sq/) with the following https://doi.org/10.17605/OSF.IO/DK8SQ. The data are available without any restricted access. The raw data are available under the file name “raw_data.csv”. The processed data are available under the file name “spermFinalAllData.csv”. The data used to produce the manuscript figures are provided in the Source Data file. Source data are provided in this paper.

Code availability
All associated code can be found at the Open Science framework database (https://osf.io/dk8sq/) with the following https://doi.org/10.17605/OSF.IO/DK8SQ.

Funding

KS was supported by an SSE Rosemary Grant award. R.V.T. and T.P. were supported by a BBSRC Standard Grant (BB/V001256/1). S.N. was supported by an Australian Research Council (ARC) Discovery Project Grant (DP210100812). S.J. was supported by a Royal Society of New Zealand Grant. R.S.G. was supported by a NERC Independent Research Fellowship (NE/M018458/1). I.S. was supported by a Biotechnology and Biological Sciences Research Council (BBSRC) Fellowship (BB/T008881/1), a Royal Society Dorothy Hodgkin Fellowship (DHF\R1\211084), and a Wellcome Institutional Strategic Support Fund, University of Oxford (BRR00060).

Funders	Funder number
Biotechnology and Biological Sciences Research Council	BB/V001256/1, BB/T008881/1
Natural Environment Research Council	NE/M018458/1
Wellcome Trust	BRR00060
The Royal Society	DHF\R1\211084
Society for the Study of Evolution
Australian Research Council	DP210100812
Royal Society of New Zealand

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Cite this

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title = "Meta-analysis shows no consistent evidence for senescence in ejaculate traits across animals",

abstract = "Male reproductive traits such as ejaculate size and quality, are expected to decline with advancing age due to senescence. It is however unclear whether this expectation is upheld across taxa. We perform a meta-analysis on 379 studies, to quantify the effects of advancing male age on ejaculate traits across 157 species of non-human animals. Contrary to predictions, we find no consistent pattern of age-dependent changes in ejaculate traits. This result partly reflects methodological limitations, such as studies sampling a low proportion of adult lifespan, or the inability of meta-analytical approaches to document non-linear ageing trajectories of ejaculate traits; which could potentially lead to an underestimation of senescence. Yet, we find taxon-specific differences in patterns of ejaculate senescence. For instance, older males produce less motile and slower sperm in ray-finned fishes, but larger ejaculates in insects, compared to younger males. Notably, lab rodents show senescence in most ejaculate traits measured. Our study challenges the notion of universal reproductive senescence, highlighting the need for controlled methodologies and a more nuanced understanding of reproductive senescence, cognisant of taxon-specific biology, experimental design, selection pressures, and life-history.",

author = "Krish Sanghvi and Regina Vega-Trejo and Shinichi Nakagawa and Gascoigne, \{Samuel J. L.\} and Johnson, \{Sheri L.\} and Roberto Salguero-G{\'o}mez and Tommaso Pizzari and Irem Sepil",

note = "We are extremely grateful to all the researchers who provided us with unpublished/missing data and life tables for various species, without whom our meta-analysis would not be possible: Abdallah Assiri, Adolfo Cordero, Adrienne Crosier, Alberto Velando, Alfonso Bolarin, Aline Malawey, Alistair Senior, Anders Pape Moller, Anil Kumar, Antje Girndt, Ashley Watt, Asim Orem, Bradley Metz, Bryan Neff, Budhan Pukazhenthi, Charles Fox, Chris Friesen, Chris Weldon, Christine Miller, Christophe Bressac, Claudia Fricke, Claudio Maia, Claus Wedekind, Clelia Gasparini, Clint McDonald, Craig Packer, Daniel Sasson, Davnah Payne, Diana Perez Staples Folger, Martha Reyez Hernandez, Distl Ottmar, Elena Zambrano, Emily “Becky” Cramer, Emily Duval, Erin MacCartney, Felipe Martinez, Fumio Hayashi, Gabriele Sorci, Gerard Wilkinson, Gerlind Lehmann, Gregor Majdic, Hasan Sevgili, Heriberto Martinez, Ilie Racotta, Ioannis Tsakmakidis, Jan Lifjeld, Jane Hurst, Janice Bailey, Maurice Clotilde, Jesus Dorado, Jurgen Heinze, Karen Lockyear, Karolina Stasiak, Katarzyna Kotarska, Kathrin Langen, Klaus Reinhardt, Leandro Miranda, Leslie Curren, Linda Penfold, Maira Brito, Malgorzata Kruczek, Manasi Kanuga, Marion Mehlis, Mark Elgar, Martin Brinkworth, Martin Schulze, Maud Bonato, Megan Head, Melissah Rowe, Michael Greenfield, Michael Ritchie, Michele Di Iorio, Michelle Helinski, Milos Krist, Moira O{\textquoteright}Bryan, Muhammed Ines Inanc, Naomi Pierce, Nicolaia Iaffaldano, Nikos Papadopolous, Nikron Thongtip, Nils Cordes, Nucharin Songsasen, Megan Brown, Pablo Bermejo Alvares, Paco Garcia Gonzales, Panos Milonas, Patricia Diogo, Paul Joseph, Philip Downing, Priscilla Ramos, Rakesh Seth, Stuart Reynolds, Rebecca Dean, Sachiko Koyama, Satoshi Hiroyoshi, Silvia Cerolini, Sina Metzler, Stanislaw Kondrack, Stefan Luepold, Steven Ramm, Stuart Meyers, Theo Bakker, Tobias Kehl, Triin Hallap, Ulrike Luderer, Upama Aich, Wael Farag, Wei Shi, Wen Liao, Xiaoxu Li, Yasaman Alavi, Yih Fwu Lin, and Yingmei Zhang. We are also thankful to Milan Vrtilek, Rose O{\textquoteright}Dea, Kevin Foster, Ana Silva, and Ellie Bath for their helpful comments and suggestions, as well as members of the Biology of Sperm Conference, 2023, for constructive criticism. Finally, we thank Neil Gemmell who supported preliminary meta-analytic investigations conducted by SJ and SN. ",

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AB - Male reproductive traits such as ejaculate size and quality, are expected to decline with advancing age due to senescence. It is however unclear whether this expectation is upheld across taxa. We perform a meta-analysis on 379 studies, to quantify the effects of advancing male age on ejaculate traits across 157 species of non-human animals. Contrary to predictions, we find no consistent pattern of age-dependent changes in ejaculate traits. This result partly reflects methodological limitations, such as studies sampling a low proportion of adult lifespan, or the inability of meta-analytical approaches to document non-linear ageing trajectories of ejaculate traits; which could potentially lead to an underestimation of senescence. Yet, we find taxon-specific differences in patterns of ejaculate senescence. For instance, older males produce less motile and slower sperm in ray-finned fishes, but larger ejaculates in insects, compared to younger males. Notably, lab rodents show senescence in most ejaculate traits measured. Our study challenges the notion of universal reproductive senescence, highlighting the need for controlled methodologies and a more nuanced understanding of reproductive senescence, cognisant of taxon-specific biology, experimental design, selection pressures, and life-history.

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Meta-analysis shows no consistent evidence for senescence in ejaculate traits across animals

Abstract

Bibliographical note

Data Availability Statement

Funding

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