Parental age at conception on mouse lemur’s offspring longevity: Sex-specific maternal effects

PLOS ONE RESEARCH ARTICLE Parental age at conception on mouse lemur’s offspring longevity: Sex-specific maternal effects Perret Martine ID*, Anzeraey Aude UMR 7179, Adaptive mechanisms and Evolution, MECADEV, Brunoy, France * Abstract a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 OPEN ACCESS Citation: Martine P, Aude A (2022) Parental age at conception on mouse lemur’s offspring longevity: Sex-specific maternal effects. PLoS ONE 17(12): e0265783. https://doi.org/10.1371/journal. pone.0265783 Editor: Heidi A. Tissenbaum, University of Massachusetts Medical School, UNITED STATES Parental age at conception often influences offspring’s longevity, a phenomenon referred as the “Lansing effect” described in large variety of organisms. But, the majority of the results refer to the survival of juveniles, mainly explained by an inadequate parental care by the elderly parents, mostly the mothers. Studies on the effect of parental age on offspring’s longevity in adulthood remain few, except in humans for whom effects of parental age vary according to statistical models or socioeconomic environments. In a small primate in which the longevity reaches up to 13 years, we investigated the effects of parental age at conception on the longevity of offspring (N = 278) issued from parents with known longevity. None of the postnatal parameters (body mass at 30 and 60 days after birth, size and composition of the litter) influenced offspring’s longevity. Mothers’ age at conception negatively affected offspring’s longevity in males but not in females. By contrast, fathers’ age at conception did not influence offspring’s longevity. Finally, the longevity of female offspring was significantly positively related to the longevity of both parents. Compared with current studies, the surprisingly minor effect of fathers ‘age was related to the high seasonal reproduction and the particular telomere biology of mouse lemurs. Received: March 7, 2022 Accepted: November 22, 2022 Published: December 29, 2022 Copyright: © 2022 Martine, Aude. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: Data are available on request from the IBISA Platform (UMR 7179, F91800 Brunoy, mail to ). Funding: The authors received no specific funding for this work. Competing interests: The authors have declared that no competing interests exist. Introduction Longevity varies greatly among individuals and increasing evidence suggests that parental age affects longevity of offspring: the longevity of offspring of older parents is shorter than that of the offspring of younger parents. This phenomenom referred as the “Lansing effect” has been decribed in many taxa including more than 300 species [1, 2]. The underlying mechanisms mainly rely on the age-related changes of germ cells and particularly of telomeres [3, 4]. However, the majority of results confirming the “Lansing effect” refer to juveniles’ survival, which is mainly explained by an inadequate parental care of aged parents. Depending on the father’s role in parental care, sex differences exist for the effects of mothers ‘age on juveniles’ survival. In birds, juveniles’ survival may be favored by older females, but it also largely depends on the resources provided by the father [5–9]. In fact, the influence of parent’s age can be reduced, even absent, when the environmental conditions are favorable. PLOS ONE | https://doi.org/10.1371/journal.pone.0265783 December 29, 2022 1 / 12 PLOS ONE Parental age at conception and offspring longevity In mammals, most of studies refer to the negative effects of mothers’ age on the pre-adult survival [2], whereas a few studies reported the role of the paternal age at conception on offspring survival [10, 11]. In humans, numerous recent studies have tested the “Lansing effect” on pre-industrial populations [10, 11] or on modern societies [12–14]. Despite extremely large samples (from 10.000 to more than five millions of people), contradictory results on the effects of parental age on the longevity of children were described, either negative or positive, depending on the statistical models, on the methods used or on the socio-economic environment to which the lengthening human longevity plays a preponderant role [15, 16]. Among non-human primates, studies on the effects of parental age on adult survival remain rare because of their great longevity and their low reproduction rate. By contrast, Malagasy prosimians constitute a more suitable model owing to their higher reproduction rate and their lower longevity. Among Malagasy species, juvenile survival until weaning is maximal when mothers are middle-aged but rapidly decreases reaching less than 20% for oldest females [17– 19]. However, few studies investigated the relationship between parent’s age and longevity of offspring at adulthood. To test the “Lansing effect”, we focused on the grey mouse lemur, a Malagasy primate. In captivity, although individuals who survived past 16 years have been recorded [20], its longevity may reach up to 13 years [21] with a median lifespan averaging 5.5 years [22]. Mouse lemurs are strict long-day photoperiodic breeders [23]. At the beginning of the breeding season, females enter oestrus and males compete to priority access to females [24]. Females give birth to 1 to 3 offspring after a 2-month gestation period and nurse infants for approximately 40 days without male parental care. Records of ages at conception for both mothers and fathers and the relative long longevity of captive mouse lemurs give the opportunity to test the “Lansing effect”. Using a large database on captive mouse lemur’s life history traits, the aim of this study was to examine whether parental age at conception affects the longevity of offspring. We expected a reduced longevity of offspring born from old parents. Finally we tested the potential relationship between parents’ and offspring’s longevity. Material and methods Animals To investigate the effects of parental age at conception on offspring lifespan, we analysed the longevity data of mouse lemurs for which the age of both parents at the time of reproduction was known. Data were recorded in the mouse lemur history traits database from a laboratory breeding colony established in Brunoy (UMR 7179 MNHN-CNRS, IBISA Platform, agreement F91.114.1, DDPP Essonne, France) from a stock originally caught near the southern western coast of Madagascar sixty years ago. Captive conditions were maintained constant with respect to ambient temperature (24– 26˚C) and hygrometry (55–60%). Animals were fed ad libitum on a standardized diet, including fresh fruits, a homemade milky mixture (19.3% proteins, 17.2% lipids and 63.5% carbohydrates) and mealworms. To ensure seasonal reproductive rhythms, animals were (...truncated)