How to generate and test hypotheses about colour: insights from half a century of guppy research.

Coloration facilitates evolutionary investigations in nature because the interaction between genotype, phenotype and environment is relatively accessible. In a landmark set of studies, Endler addressed this complexity by demonstrating that the evolution of male Trinidadian guppy coloration is shaped by the local balance between selection for mate attractiveness versus crypsis. This became a textbook paradigm for how antagonistic selective pressures may determine evolutionary trajectories in nature. However, recent studies have challenged the generality of this paradigm. Here, we respond to these challenges by reviewing five important yet underappreciated factors that contribute to colour pattern evolution: (i) among-population variation in female preference and correlated variation in male coloration, (ii) differences in how predators versus conspecifics view males, (iii) biased assessment of pigmentary versus structural coloration, (iv) the importance of accounting for multi-species predator communities, and (v) the importance of considering the multivariate genetic architecture and multivariate context of selection and how sexual selection encourages polymorphic divergence. We elaborate these issues using two challenging papers. Our purpose is not to criticize but to point out the potential pitfalls in colour research and to emphasize the depth of consideration necessary for testing evolutionary hypotheses using complex multi-trait phenotypes such as guppy colour patterns.

Replicated origin of female-biased adult sex ratio in introduced populations of the trinidadian guppy (Poecilia reticulata).

There are many theoretical and empirical studies explaining variation in offspring sex ratio but relatively few that explain variation in adult sex ratio. Adult sex ratios are important because biased sex ratios can be a driver of sexual selection and will reduce effective population size, affecting population persistence and shapes how populations respond to natural selection. Previous work on guppies (Poecilia reticulata) gives mixed results, usually showing a female-biased adult sex ratio. However, a detailed analysis showed that this bias varied dramatically throughout a year and with no consistent sex bias. We used a mark-recapture approach to examine the origin and consistency of female-biased sex ratio in four replicated introductions. We show that female-biased sex ratio arises predictably and is a consequence of higher male mortality and longer female life spans with little effect of offspring sex ratio. Inconsistencies with previous studies are likely due to sampling methods and sampling design, which should be less of an issue with mark-recapture techniques. Together with other long-term mark-recapture studies, our study suggests that bias in offspring sex ratio rarely contributes to adult sex ratio in vertebrates. Rather, sex differences in adult survival rates and longevity determine vertebrate adult sex ratio.

Size-fecundity relationships, growth trajectories, and the temperature-size rule for ectotherms.

Many ectotherms show crossing growth trajectories as a plastic response to rearing temperature. As a result, individuals growing up in cool conditions grow slower, mature later, but are larger at maturation than those growing up in warm conditions. To date, no entirely satisfactory explanation has been found for why this pattern, often called the temperature-size rule, should exist. Previous theoretical models have assumed that size-specific mortality rates were most likely to drive the pattern. Here, I extend one theoretical model to show that variation in size-fecundity relationships may also be important. Plasticity in the size-fecundity relationship has rarely been considered, but a number of studies show that fecundity increases more quickly with size in cold environments than it does in warm environments. The greater increase in fecundity offsets costs of delayed maturation in cold environments, favoring a larger size at maturation. This can explain many cases of crossing growth trajectories, not just in relation to temperature.

Juvenile compensatory growth has negative consequences for reproduction in Trinidadian guppies (Poecilia reticulata).

Compensatory or 'catch-up' growth may be an adaptive mechanism that buffers the growth trajectory of young organisms from deviations caused by reduced food availability. Theory generally assumes that rapid juvenile compensatory growth impacts reproduction only through its positive effects on age and size at maturation, but potential reproductive costs to juvenile compensatory growth remain virtually unexplored. We used a food manipulation experiment to examine the reproductive consequences of compensatory growth in Trinidadian guppies (Poecilia reticulata). Compensatory growth did not affect adult growth rates, litter production rates or investment in offspring size. However, compensatory growth had negative effects on litter size, independent of the effects of female body length, resulting in a 20% decline in offspring production. We discuss potential mechanisms behind this observed cost to reproduction.

Influence of sprint speed and body size on predator avoidance in New Mexican spadefoot toads (Spea multiplicata).

Predator-prey interactions play an important role in community dynamics and may be important for promoting genetic diversification. Diversification may be especially important when prey species have multiple anti-predator strategies available, but these strategies conflict with each other. For example, rapid sprint speed and large size are both thought to decrease vulnerability to many predators. A physiological trade-off between swimming speed and growth rate has been documented in many aquatic species and, as a result, individual genotypes may employ one strategy or the other, but not both. Although rapid sprint speed is often assumed to decrease vulnerability to predators, this has only rarely been tested. Here I provide evidence that both rapid sprint speed and large size in tadpoles of the New Mexico spadefoot toad (Spea multiplicata) decreases predation risk from carnivore morphs of its congener the Great Plains spadefoot toad (Spea bombifrons). Such conflicts, coupled with spatio-temporal variation in predation pressure, may be important in maintaining genetic variation for trade-offs.

Evolution of juvenile growth rates in female guppies (Poecilia reticulata): predator regime or resource level?

Recent theoretical and empirical work argues that growth rate can evolve and be optimized, rather than always being maximized. Chronically low resource availability is predicted to favour the evolution of slow growth, whereas attaining a size-refuge from mortality risk is predicted to favour the evolution of rapid growth. Guppies (Poecilia reticulata) evolve differences in behaviour, morphology and life-history traits in response to predation, thus demonstrating that predators are potent agents of selection. Predators in low-predation environments prey preferentially on small guppies, but those in high-predation environments appear to be non-selective. Because guppies can outgrow their main predator in low- but not high-predation localities, we predict that predation will select for higher growth rates in the low-predation environments.However, low-predation localities also tend to have lower productivity than high-predation localities, yield-ing the prediction that guppies from these sites should have slower growth rates. Here we compare the growth rates of the second laboratory-born generation of guppies from paired high- and low-predation localities from four different drainages. In two out of four comparisons, guppies from high-predation sites grew significantly faster than their low-predation counterparts. We also compare laboratory born descendants from a field introduction experiment and show that guppies introduced to a low-predation environment evolved slower growth rates after 13 years, although this was evident only at the high food level. The weight of the evidence suggests that resource availability plays a more important role than predation in shaping the evolution of growth rates.

OPTIMISTIC GROWTH: COMPETITION AND AN ONTOGENETIC NICHE-SHIFT SELECT FOR RAPID GROWTH IN PUMPKINSEED SUNFISH (LEPOMIS GIBBOSUS).

Intrinsic growth rate is emerging as an important life-history trait that can be modified by natural selection. One factor determining optimal intrinsic growth rates is the pattern of resource availability. Organisms that experience chronically low resource levels tend to have slow intrinsic growth rates. However, this does not necessarily hold if resource levels change as an organism grows. We present a theoretical model showing that rapid growth is favored when resource levels for small size classes are low relative to resource levels for large size classes. We call such a growth strategy "optimistic" because rapid growth is based on an expectation that resources will improve once a minimum size is reached. We provide empirical support for this hypothesis by examining the intrinsic growth rates of pumpkinseed sunfish derived from three populations sympatric with bluegill sunfish (an important competitor with small size classes) to three populations allopatric with bluegill sunfish raised under common conditions. Rapid growth has evolved in the sympatric fish to reach the size refuge from competition as quickly as possible.