Decades of field data reveal that turtles senesce in the wild

Survival senescence has generally been thought to be negligible or absent in various reptiles (refs. 23–27) but see ref. 3) because traits that either protect against predators (such as external ribcages and venom; reviewed in ref. 28) or that increase reproductive success with advancing age (such as indeterminate growth and fecundity) may overcome the declining power of natural selection with advancing age that characterizes natural populations (10, 14). In the specific case of C. picta, which has both adult-protective morphology and indeterminate growth and fecundity, lifetime fitness would increase if individuals maintained successful and increasing reproduction through adulthood. Such steady or even increasing reproduction with advancing age is particularly likely for species that exhibit low rates of extrinsic mortality at old ages, indeterminate growth, or a positive relationship between body size and fecundity (e.g., ref. 26) [i.e., many reptiles, including turtles (27)]. Although our aim was to understand whether and how indeterminate growth and fecundity may offset declining late-life selection, our 24-y dataset on C. picta revealed instead a significant decline in both reproductive success and adult survival for females. Moreover, when we tested among competing models for mortality acceleration, some of which would allow deceleration later in life, the Gompertz model had the most support (Table 2), suggesting increasing mortality acceleration over the entire adult lifespan (Fig. 4).

Our results differ from those for another C. picta population, which exhibits both overall low mortality and no differences in survivorship of old- versus middle-aged females (23). Although the survivorship curves of ref. 23 are consistent with gently increasing mortality with advancing age in that population, for direct tests of senescence, it is important to estimate and analyze age-specific mortality hazards as we have done here (29). Thus, estimating the rate and form of mortality senescence by computing instantaneous mortality rates revealed that the present study population of C. picta is characterized by mortality senescence (i.e., accelerating mortality with advancing age). Our study population differs from that of ref. 23 in that ours has experienced a relatively long history of human-driven mortality. The extent to which this human-induced mortality is in any way age-dependent is unknown. Specific human-induced mortality derives primarily from injuries to nesting females (e.g., when crossing roads) and injuries to adults of both sexes in the water column (e.g., by boating activity). Were these injuries to manifest in an age-dependent manner across the lifespan, the age-specific selection gradients could be altered. In contrast, if the increased mortality affected all adult ages equally, we would expect acceleration of the entire life history, because the population age structure would become skewed toward young ages. A comparison of the high mortality population (this study) and a lower mortality population (23) supports this contention. Specifically, here we detected rapid young-adult growth rates (Fig. S5), increased reproductive effort at young adult ages, and reduced lifespan of turtles in our population. Moreover, extensive demographic analyses of prematuration growth in our population indicated faster individual growth and earlier maturation than in less human-impacted populations (30). Thus, these two painted turtle populations fit strikingly well with predictions from life-history theory based on the force and sensitive ages of mortality (14, 31) (Fig. S4). Overall then, these studies support the notion that the life-history strategy is a set of correlated traits that respond predictably to natural selection.

Interestingly, in contrast to reproduction and survival, measures related to body size and behavior did not exhibit senescence (Fig. 1 and Fig. S5). This result accords with evolutionary senescence theory in that such traits (i.e., growth and learning, respectively) could buffer selective forces that accelerate death and infertility rates (9, 32). At the same time, hatching success and adult mortality—traits that are substantially influenced by physiological processes (27)—exhibited senescence. Long-term research that not only assesses shifts in survival and reproductive parameters with age but also quantifies age-related changes in physiology and offspring fitness may reveal that senescent patterns in long-lived reptiles are common (see also refs. 33, 34). In addition, long-term studies that explore tradeoffs between early- and late-life performance will provide crucial information for better understanding these declines in reproduction or survival as individuals age. For example, greater resource allocation to early-life growth or reproduction is expected to come at a cost to late-life performance that can lead to age-related declines in reproduction and survival [i.e., disposable soma theory of aging (35)]. These patterns have been observed in many vertebrates (36), including reptiles (37, 38), and could contribute to the reproductive and survival senescence observed here in C. picta.

Determining the universality of reproductive aging has received great recent interest both in terms of documenting its existence and calculating whether reproductive aging occurs at similar (vs. faster) rates than general senescence (13). Analyses have taken the form of either measuring the rate of declining fertility and reproductive success with advancing age (39, 40) or measuring the distribution of ages of last successful reproduction and comparing that to the distribution of deaths (16). Our analysis is similar to the former of these approaches, and we indeed document reproductive decline with advancing age, although not in measures traditionally used (such as rates of conception) but rather by calculating egg-hatching success. Similarly, Congdon et al. (24) reported greater embryo mortality attributable to arrested development in eggs produced by the oldest female age class in Blanding’s turtles. Other long-lived species tend to exhibit reproductive senescence at rates that are faster than somatic aging and that ends at an earlier age than death, which yields a postreproductive lifespan [primates including humans (16), killer whales (41), but see elephants (42, 43)]. These mammalian species may exhibit reproductive senescence attributable to a shelf-life of their primary oocytes, but this possibility is unlikely the case in C. picta because reptiles are not oocyte-limited (44). One firm conclusion is that reproductive senescence in turtles and other ectothermic amniotes cannot be attributable to adaptive explanations invoked in the mammalian literature [e.g., the “grandmother hypothesis,” which largely rests on the role of parental care to increase one’s own fitness or the fitness of relatives (45)].

A critical question is whether senescent changes in mortality (as in primates) or in reproduction drive declines in fitness. In reptiles, which are often characterized as indeterminate growers, few studies document either mortality senescence or the decline in some physiological trait with advancing adult age (3). Because many species with indeterminate growth increase fecundity with increasing age (attributable in part to increasing body size), the question becomes, at what level of increased fecundity will selection cease declining with advancing age? Although we demonstrate mortality senescence in our population of C. picta, the age-specific increase in mortality is considerably less rapid than that reported for mammalian taxa (e.g., Fig. 4), which is consistent with the view that rates of senescence in these long-lived reptiles are relatively slow. These divergent patterns may be explained by very different rates of extrinsic mortality in turtles (or their ancestors) compared with mammals. Indeed, because of their protective morphology (shell) and lack of senescence in immune function (46), turtles likely experience considerably less late-age mortality attributable to extrinsic factors than do mammals. This comparison between turtles and mammals fits with theoretical expectations for patterns of survival senescence in these taxa, but our results challenge the traditional view that long-lived ectotherms, such as turtles, do not exhibit declining reproductive function with advancing age. Indeed, declines in fitness with age will be exacerbated by a combination of increased mortality rate and decreased reproductive success, as we demonstrate in these long-lived ectotherms.

Since 1988, nesting patterns of painted turtles (C. picta) have been continually monitored at the Thomson Causeway Recreation Area in northwestern Illinois (Carroll County; 41°57′N, 90°7′W) (10–12). Unmarked females exhibiting 5–7 annuli on the pectoral scutes were classified as primiparous (i.e., a reproductive age of one, chronological age 5–7 y old). Thus, all future recaptures of these animals were at a known age (20). Individuals that could not be assigned ages confidently were excluded from analyses of reproduction unless the turtles were recaptured across a 15+ y time span, in which case, data collected from captures ≥15 y after initial capture were included in the oldest age class (i.e., chronological age ≥20 y old). During each nesting season (mid-May to early July), the study area was monitored intensively for nesting turtles. All females at the nesting grounds were individually marked, and their eggs were weighed and counted (typically within 4 h of oviposition). All eggs were returned to their nests and allowed to incubate naturally, and nests were checked for predation almost daily until the end of June of each year. Microhabitat data (shade cover and distance from the water) were also collected for each nest to assess age-related changes in nesting behavior. Nesting behaviors are important because maternal choice of nest microhabitat differs among age classes (47) and can influence egg survival (18). These data are available in the Dryad Digital Repository (dx.doi.org/10.5061/dryad.g2r87).

This research has been approved by the Iowa State University Institutional Animal Care and Use Committee and the Illinois Department of Natural Resources.

We thank the many volunteers, students, and postdoctoral researchers who have been involved with fieldwork at Turtle Camp over the past decades. We thank members of F.J.J.’s laboratory and T. Schwartz for helpful comments on earlier drafts of this paper and J. Sherwood for assistance with ArcGIS software. We acknowledge ongoing support from the US Fish and Wildlife Service and the US Army Corp of Engineers. Funding for this research was provided by National Science Foundation Grants DEB-9629529, DEB-0089680, DEB-0640932, and DEB-1242510 (to F.J.J.). Additional support was provided by a National Institutes of Health Grant R01AG049416.