High reproductive effort is associated with decreasing mortality late in life in captive ruffed lemurs

Abstract

Evolutionary theories of senescence predict that a high allocation to reproduction during early life should have long-term deleterious consequences on future reproduction or survival because individuals have to face an energy allocation trade-off between reproductive effort and the maintenance of body condition. Using a high-quality dataset from 1,721 red ruffed lemurs (RRL, Varecia rubra) and 3,637 black and white ruffed lemurs (BWRM, V. variegata) living in captivity, we tested the existence of a trade-off between reproductive effort and late-life survival after accounting for possible confounding effects of natal environmental conditions. We report clear evidence of actuarial senescence (i.e., the decline of annual survival with increasing age) in both sexes and for both species of ruffed lemurs. RRL had a lower baseline mortality and senesced faster than BWRL, resulting in similar distributions of longevities for both species. No between-sex difference was observed in any species. Lastly, a higher reproductive effort was positively associated with an increase of survival late in life, and thereby an increased longevity. These findings indicate that individual quality rather than trade-off drives the association between reproductive success and survival pattern among individual lemurs of both species in the protected environment provided by zoos. Lemurs are among the world's highest conservation priorities and better understanding factors influencing their longevity and actuarial senescence patterns should improve their conservation.

Female reproduction bears no survival cost in captivity for gray mouse lemurs

“…Former studies on other captive populations of vertebrates reached the same conclusion: no evidence of survival cost of reproduction could be found (Kengeri et al, ; Ricklefs & Cadena, ; Tarin et al, ; Tidière et al, ). For instance, Tidière et al, failed to detect a negative impact of reproduction on survival using a sample of 5,358 ruffed lemurs kept in a zoo. However, all referred former studies (including Tidière et al, ) had little opportunity for properly controlling for variance in resource acquisition, either through time or between individuals.…”

“…For instance, Tidière et al, failed to detect a negative impact of reproduction on survival using a sample of 5,358 ruffed lemurs kept in a zoo. However, all referred former studies (including Tidière et al, ) had little opportunity for properly controlling for variance in resource acquisition, either through time or between individuals. The present study does control for various confounding variables and suggests that the lack of CoR in former studies is actually a true lack of CoR and not a spurious conclusion due to hidden sources of heterogeneity that had not been properly accounted for in statistical analyses.…”

“…Studies on zoo populations for 18 mammal and 12 bird species (Ricklefs & Cadena, ), on Rottweiler pet dogs (Kengeri, Maras, Suckow, Chiang, & Waters, ) and laboratory mice (Tarin, Gomez‐Piquer, Garcia‐Palomares, Garcia‐Perez, & Cano, ), have actually failed to detect any CoR. Positive relationship between reproductive effort and survival was even found in ruffed lemurs kept in zoos (Tidière, Lemaître, Douay, Whipple, & Gaillard, ).…”

“…But because these covariates cannot explain all interindividual variance, it is necessary to also take into account the residual interindividual variability by adding random effects in the analyses (Plard et al, ). Former studies did not have detailed individual information (such as health, lineage, or body mass), and thus were not able to unambiguously conclude the absence of CoR in captive populations (Kengeri et al, ; Ricklefs & Cadena, ; Tarin et al, ; Tidière et al, ).…”

Disentangling Pre- and Postnatal Maternal Age Effects on Offspring Performance in an Insect with Elaborate Maternal Care

“…There are many advantages to measuring senescence in laboratory populations, but it is not clear to what degree laboratory findings fairly represent aging in natural populations. Comparative research involving invertebrate and mammal species has shown the importance of contrasting laboratory/zoo and wild aging rates, as the two can be extremely different (Bonduriansky and Brassil 2002;Carey et al 2008;Dukas 2008;Kawasaki et al 2008;Rodríguez-Muñoz et al 2010;Sherratt 2010;Tidière et al 2017). One likely contribution to these differences is that laboratory conditions are relatively benign and free from physiological stressors, such as the need to locate and defend a resource (Scott 1998).…”