Classical theories for the evolution of senescence predict that organisms that experience low mortality rates attributable to external factors, such as disease or predation, will evolve a later onset of senescence. Here we use patterns of senescence in guppies derived from natural populations that differ in mortality risk to evaluate the generality of these predictions. We have previously found that populations experiencing higher mortality rates evolve earlier maturity and invest more in reproduction, as predicted by evolutionary theory. We report here that these same populations do not have an earlier onset of senescence with respect to either mortality or reproduction but do with respect to swimming performance, which assesses neuromuscular function. This mosaic pattern of senescence challenges the generality of the association between decreased extrinsic mortality and delayed senescence and invites consideration of more derived theories for the evolution of senescence.

The theory of rand K-selection was one of the first predictive models for life-history evolution. It helped to galvanize the empirical field of comparative life-history and dominated thinking on the subject from the late 1960s through the 1970s. Large quantities of field data were collected that claimed to test predictions of the theory. By the early 1980s, sentiment about the theory had changed so completely that a proposal to test it or the use of it to interpret empirical results would likely be viewed as archaic and naïve. The theory was displaced by demographic models that concentrated on mortality patterns as the cause of life-history evolution. Although demographic models are known for their density-independent approach and focus on extrinsic mortality, these models can incorporate many ecological features captured by rand K-selection, such as density-dependent population regulation, resource availability, and environmental fluctuations. We highlight the incorporation of these factors in recent theory, then show how they are manifest in our research on life-history evolution in Trinidadian guppies (Poecilia reticulata). Explanations of the repeatable suites of life-history differences across populations of guppies originate from demographic models of predator-driven age-specific mortality. Recently, careful examination of guppy demography and habitat has revealed that density-dependent regulation and resource availability may have influenced the evolution of guppy life histories. In the field, these factors covary with predation risk; however, they can be uncoupled experimentally, providing insight into how they may have synergistically driven guppy life-history evolution. Although life-history theory has shifted away from a focus on rand K-selection, the themes of density-dependent regulation, resource availability, and environmental fluctuations are integral to current demographic theory and are potentially important in any natural system.

Life history traits in guppies (Poecilia reticulata) vary geographically along a predator assemblage gradient, and field experiments have indicated that the association may be causal; guppies introduced from high predation sites to low predation sites have evolved the phenotype associated with low predation in as few as seven generations. It has long been recognized, however, that low predation sites tend to have greater forest canopy cover than high predation sites. Stream differences in canopy cover could translate into stream differences in resource availability, another theoretically potent agent of selection on life history traits. Moreover, new computer simulations indicate that the high predation phenotype would outcompete the low predation phenotype under both mortality regimes. Thus, predation alone may not be sufficient to explain the observed life history patterns.Here we show that food availability for guppies decreases as forest canopy cover increases, among six low predation streams in the Northern Range of Trinidad. Streams with less canopy cover received more photosynthetically active light and contained a larger standing crop of algae (the primary food of guppies), as measured by algal pigments (chlorophylls and carotenoids) on both natural cobble and artificial tile substrates, but did not contain a greater biomass of guppies (per square meter of streambed). Consequently, algae availability for guppies (in micrograms of algal pigments per milligram of guppy) increased with decreasing canopy cover. The biomass of guppies and algae both decreased after a series of floods, with no net effect on algae availability. Field mark-recapture studies revealed that female and juvenile guppies grew faster, and that the asymptotic size of mature males was larger, in streams with less canopy cover. Canopy cover explained 84% of the variation among streams in algae availability which, in turn, explained 93% of the variation in guppy growth rates. Laboratory ''common garden'' experiments indicated that the stream differences in growth and adult male size in the field were largely environmental (nongenetic). These results strongly suggest that stream differences in canopy cover result in consistent stream differences in food availability, independent of predation.Our preliminary data indicate that some life history traits (offspring size and litter size) vary genetically along the canopy cover gradient, among low predation streams, in the same direction as along the predation gradient. Another recent study shows that food availability is higher at high predation sites than at low predation sites, partly as an indirect effect of predators reducing guppy densities. Further research is required to disentangle the direct effects of predation from those of resource availability in the evolution of life histories.

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