Fitness costs of reproduction depend on life speed: empirical evidence from mammalian populations

Abstract

Fitness costs of reproduction play a key role in understanding the evolution of reproductive tactics. Nevertheless, the detection and the intensity of costs of reproduction vary according to which life-history traits and species are studied. We propose an evolutionary model demonstrating that the chance of detecting a cost of reproduction should be lower when the fitness component studied has a low rather than high variance. Consequently, the fitness component that is affected the most by costs of reproduction should vary with life speed. Since long-lived species have developed a strategy that avoids jeopardizing their survival and short-lived species favour current reproduction, variance in survival is smaller and variance in reproduction higher in long-lived vs. short-lived species. We review empirical studies of costs of reproduction in free-ranging mammals, comparing evidence of costs reported among species and focal traits. In support of our model, more studies reported evidence of reproductive costs of reproduction in ungulates than in rodents, whereas survival costs of reproduction were more frequent in rodents than in ungulates. The life-history model we propose is expected to apply to any species, and hence provides a better understanding of life-history variation, which should be relevant to all evolutionary ecologists. KeywordsEnvironmental canalization, investment, mammals, reproductive tactics, resource acquisition, resource allocation, rodents, ungulates, van Noordwijk and de JongÕs model, variable environment.Ecology Letters (2010) 13: 915-935 Positive or negative co-variations among fitness components are central to life-history theory (Stearns 1992). The notion of negative co-variations originates from the principle of allocation (Williams 1966), which posits that resources available for an individual are limited, so that individuals should allocate resources optimally among growth, survival, and reproduction in order to maximize their fitness (Stearns 1992). As reproduction requires high energy allocation (Robbins 1993), fitness costs of reproduction (see Box 1 for definitions) should occur and lead to negative co-variations between current reproduction and future survival and ⁄ or reproduction (Stearns 1992;Roff 2002). Williams (1966) was the first to introduce this cost-benefit concept of reproduction, which was further developed by numerous authors (e.g. Gadgil & Bossert 1970;Bell 1980;Reznick et al. 2000). Costs of reproduction have received a particular attention in the literature because they play a key role in the evolution of reproductive tactics (Roff 2002). They can also have fundamental demographic consequences on population dynamics by decreasing reproduction and survival, and thereby changing the population age structure and growth rate (Silvertown & Dodd 1999;Proaktor et al. 2008).As energy allocation is particularly important during gestation and lactation (Gittleman & Thompson 1988), mammals are relevant model species to assess costs of reproduction. In his review of ...

Reproductive costs in terrestrial male vertebrates: insights from bird studies

“…Moreover, as highlighted for female mammals, a close relationship between pace of life and the type of direct reproductive costs detected may be expected (i.e. fast species should be affected by survival costs of reproduction, whereas slow species by fecundity costs of reproduction [6]). Generation time provides a relevant measure to rank the species on the fast-slow continuum [17].…”

“…More recently, studies investigating specifically direct reproductive costs in wild mammals-the covariations between current reproduction (at time t) and subsequent reproduction and/or survival (at time t þ 1)-have been reviewed [6]. Interestingly, most of the studies gathered in this review focused on females [6]. There have in fact been considerably fewer attempts to assess trade-offs among fitness components in wild males.…”

“…While a high level of polygyny or paternal care is expected to be costly for males, such costs of reproduction can also strongly depend upon the position of the species on the fast -slow continuum of life-history variation [16,17]. Indeed, the recent extension of van Noordwijk & de Jong's model [5] predicts that reproductive costs are closely linked to the position of a given species on the fast -slow continuum [6], which contrasts fast species with early maturity, high fecundity and short lifespan to slow species with opposite characteristics (see [18] for a recent review). Briefly, (iii) fast species characterized with high variance in survival and low variance in reproduction should exhibit survival costs of reproduction, whereas slow species should rather suffer from fecundity costs.…”

“…Briefly, (iii) fast species characterized with high variance in survival and low variance in reproduction should exhibit survival costs of reproduction, whereas slow species should rather suffer from fecundity costs. While this evolutionary model has been first supported in female mammals [6], its validity for male vertebrates remains to be investigated.…”

“…Stearns reviewed studies investigating the effects of reproduction on growth, parental survival, late fecundity and longevity in a wide range of taxa and with different methods, including laboratory experiments, unmanipulated and manipulated field populations [1]. More recently, studies investigating specifically direct reproductive costs in wild mammals-the covariations between current reproduction (at time t) and subsequent reproduction and/or survival (at time t þ 1)-have been reviewed [6]. Interestingly, most of the studies gathered in this review focused on females [6].…”