Sex-specific aging in animals: Perspective and future directions

Anne M Bronikowski; Richard P Meisel; Peggy R Biga; James R Walters; Judith E Mank; Erica Larschan; Gerald S Wilkinson; Nicole Valenzuela; Ashley Mae Conard; João Pedro de Magalhães; Jingyue Ellie Duan; Amy E Elias; Tony Gamble; Rita M Graze; Kristin E Gribble; Jill A Kreiling; Nicole C Riddle

doi:10.1111/acel.13542

Sex-specific aging in animals: Perspective and future directions

Aging Cell. 2022 Feb;21(2):e13542. doi: 10.1111/acel.13542. Epub 2022 Jan 23.

Authors

Anne M Bronikowski¹, Richard P Meisel², Peggy R Biga³, James R Walters⁴, Judith E Mank^{5

6}, Erica Larschan⁷, Gerald S Wilkinson⁸, Nicole Valenzuela¹, Ashley Mae Conard⁹, João Pedro de Magalhães¹⁰, Jingyue Ellie Duan¹¹, Amy E Elias⁷, Tony Gamble^{12

13

14}, Rita M Graze¹⁵, Kristin E Gribble¹⁶, Jill A Kreiling⁷, Nicole C Riddle³

Affiliations

¹ Department of Ecology, Evolution, and Organismal Biology, Iowa State University, Ames, Iowa, USA.
² Department of Biology and Biochemistry, University of Houston, Houston, Texas, USA.
³ Department of Biology, The University of Alabama at Birmingham, Birmingham, Alabama, USA.
⁴ Department of Ecology and Evolutionary Biology, The University of Kansas, Lawrence, Kansas, USA.
⁵ Department of Zoology, University of British Columbia, Vancouver, British Columbia, Canada.
⁶ Department of Bioscience, University of Exeter, Penryn, UK.
⁷ Department of Molecular Biology, Cell Biology and Biochemistry, Brown University, Providence, Rhode Island, USA.
⁸ Department of Biology, University of Maryland, College Park, Maryland, USA.
⁹ Department of Computer Science, Center for Computational and Molecular Biology, Brown University, Providence, Rhode Island, USA.
¹⁰ Integrative Genomics of Ageing Group, Institute of Ageing and Chronic Disease, University of Liverpool, Liverpool, UK.
¹¹ Department of Animal Science, Cornell University, Ithaca, New York, USA.
¹² Department of Biological Sciences, Marquette University, Milwaukee, Wisconsin, USA.
¹³ Milwaukee Public Museum, Milwaukee, Wisconsin, USA.
¹⁴ Bell Museum of Natural History, University of Minnesota, Saint Paul, Minnesota, USA.
¹⁵ Department of Biological Sciences, Auburn University, Auburn, Alabama, USA.
¹⁶ Josephine Bay Paul Center for Comparative Molecular Biology and Evolution, Marine Biological Laboratory, Woods Hole, Massachusetts, USA.

Abstract

Sex differences in aging occur in many animal species, and they include sex differences in lifespan, in the onset and progression of age-associated decline, and in physiological and molecular markers of aging. Sex differences in aging vary greatly across the animal kingdom. For example, there are species with longer-lived females, species where males live longer, and species lacking sex differences in lifespan. The underlying causes of sex differences in aging remain mostly unknown. Currently, we do not understand the molecular drivers of sex differences in aging, or whether they are related to the accepted hallmarks or pillars of aging or linked to other well-characterized processes. In particular, understanding the role of sex-determination mechanisms and sex differences in aging is relatively understudied. Here, we take a comparative, interdisciplinary approach to explore various hypotheses about how sex differences in aging arise. We discuss genomic, morphological, and environmental differences between the sexes and how these relate to sex differences in aging. Finally, we present some suggestions for future research in this area and provide recommendations for promising experimental designs.

Keywords: aging; comparative biology; lifespan; mortality; sex differences.

Publication types

Research Support, U.S. Gov't, Non-P.H.S.
Review

MeSH terms

Aging* / genetics
Animals
Female
Longevity* / genetics
Male
Sex Characteristics

Grants and funding

T32 AG041688/AG/NIA NIH HHS/United States