How differing modes of non-genetic inheritance affect population viability in fluctuating environments.

Different modes of non-genetic inheritance are expected to affect population persistence in fluctuating environments. We here analyse Caenorhabditis elegans density-independent per capita growth rate time series on 36 populations experiencing six controlled sequences of challenging oxygen level fluctuations across 60 generations, and parameterise competing models of non-genetic inheritance in order to explain observed dynamics. Our analysis shows that phenotypic plasticity and anticipatory maternal effects are sufficient to explain growth rate dynamics, but that a carryover model where 'epigenetic' memory is imperfectly transmitted and might be reset at each generation is a better fit to the data. We further find that this epigenetic memory is asymmetric since it is kept for longer when populations are exposed to the more challenging environment. Our analysis suggests that population persistence in fluctuating environments depends on the non-genetic inheritance of phenotypes whose expression is regulated across multiple generations.

Slower environmental change hinders adaptation from standing genetic variation.

Evolutionary responses to environmental change depend on the time available for adaptation before environmental degradation leads to extinction. Explicit tests of this relationship are limited to microbes where adaptation usually depends on the sequential fixation of de novo mutations, excluding standing variation for genotype-by-environment fitness interactions that should be key for most natural species. For natural species evolving from standing genetic variation, adaptation at slower rates of environmental change may be impeded since the best genotypes at the most extreme environments can be lost during evolution due to genetic drift or founder effects. To address this hypothesis, we perform experimental evolution with self-fertilizing populations of the nematode Caenorhabditis elegans and develop an inference model to describe natural selection on extant genotypes under environmental change. Under a sudden environmental change, we find that selection rapidly increases the frequency of genotypes with high fitness in the most extreme environment. In contrast, under a gradual environmental change selection first favors genotypes that are worse at the most extreme environment. We demonstrate with a second set of evolution experiments that, as a consequence of slower environmental change and thus longer periods to reach the most extreme environments, genetic drift and founder effects can lead to the loss of the most beneficial genotypes. We further find that maintenance of standing genetic variation can retard the fixation of the best genotypes in the most extreme environment because of interference between them. Taken together, these results show that slower environmental change can hamper adaptation from standing genetic variation and they support theoretical models indicating that standing variation for genotype-by-environment fitness interactions critically alters the pace and outcome of adaptation under environmental change.

Evolution of increased larval competitive ability in Drosophila melanogaster without increased larval feeding rate.

Multiple experimental evolution studies on Drosophila melanogaster in the 1980s and 1990s indicated that enhanced competitive ability evolved primarily through increased larval tolerance to nitrogenous wastes and increased larval feeding and foraging rate, at the cost of efficiency of food conversion to biomass, and this became the widely accepted view of how adaptation to larval crowding evolves in fruitflies.We recently showed that populations of D. ananassae and D. n. nasuta subjected to extreme larval crowding evolved greater competitive ability without evolving higher feeding rates, primarily through a combination of reduced larval duration, faster attainment of minimum critical size for pupation, greater efficiency of food conversion to biomass, increased pupation height and, perhaps, greater urea/ammonia tolerance. This was a very different suite of traits than that seen to evolve under similar selection in D. melanogaster and was closer to the expectations from the theory of K-selection. At that time, we suggested two possible reasons for the differences in the phenotypic correlates of greater competitive ability seen in the studies with D. melanogaster and the other two species. First, that D. ananassae and D. n. nasuta had a very different genetic architecture of traits affecting competitive ability compared to the long-term laboratory populations of D. melanogaster used in the earlier studies, either because the populations of the former two species were relatively recently wild-caught, or by virtue of being different species. Second, that the different evolutionary trajectories in D. ananassae and D. n. nasuta versus D. melanogaster were a reflection of differences in the manner in which larval crowding was imposed in the two sets of selection experiments. The D. melanogaster studies used a higher absolute density of eggs per unit volume of food, and a substantially larger total volume of food, than the studies on D. ananassae and D. n. nasuta. Here, we show that long-term laboratory populations of D. melanogaster, descended from some of the populations used in the earlier studies, evolve essentially the same set of traits as the D. ananassae and D. n. nasuta crowding-adapted populations when subjected to a similar larval density at low absolute volumes of food. As in the case of D. ananassae and D. n. nasuta, and in stark contrast to earlier studies with D. melanogaster, these crowding-adapted populations of D. melanogaster did not evolve greater larval feeding rates as a correlate of increased competitive ability. The present results clearly suggest that the suite of phenotypes through which the evolution of greater competitive ability is achieved in fruitflies depends critically not just on larval density per unit volume of food, but also on the total amount of food available in the culture vials. We discuss these results in the context of an hypothesis about how larval density and the height of the food column in culture vials might interact to alter the fitness costs and benefits of increased larval feeding rates, thus resulting in different routes to the evolution of greater competitive ability, depending on the details of exactly how the larval crowding was implemented.

Adaptation to Temporally Fluctuating Environments by the Evolution of Maternal Effects.

All organisms live in temporally fluctuating environments. Theory predicts that the evolution of deterministic maternal effects (i.e., anticipatory maternal effects or transgenerational phenotypic plasticity) underlies adaptation to environments that fluctuate in a predictably alternating fashion over maternal-offspring generations. In contrast, randomizing maternal effects (i.e., diversifying and conservative bet-hedging), are expected to evolve in response to unpredictably fluctuating environments. Although maternal effects are common, evidence for their adaptive significance is equivocal since they can easily evolve as a correlated response to maternal selection and may or may not increase the future fitness of offspring. Using the hermaphroditic nematode Caenorhabditis elegans, we here show that the experimental evolution of maternal glycogen provisioning underlies adaptation to a fluctuating normoxia-anoxia hatching environment by increasing embryo survival under anoxia. In strictly alternating environments, we found that hermaphrodites evolved the ability to increase embryo glycogen provisioning when they experienced normoxia and to decrease embryo glycogen provisioning when they experienced anoxia. At odds with existing theory, however, populations facing irregularly fluctuating normoxia-anoxia hatching environments failed to evolve randomizing maternal effects. Instead, adaptation in these populations may have occurred through the evolution of fitness effects that percolate over multiple generations, as they maintained considerably high expected growth rates during experimental evolution despite evolving reduced fecundity and reduced embryo survival under one or two generations of anoxia. We develop theoretical models that explain why adaptation to a wide range of patterns of environmental fluctuations hinges on the existence of deterministic maternal effects, and that such deterministic maternal effects are more likely to contribute to adaptation than randomizing maternal effects.

A possible mechanism for the attainment of out-of-phase periodic dynamics in two chaotic subpopulations coupled at low dispersal rate.

Much research in metapopulation dynamics has concentrated on identifying factors that affect coherence in spatially structured systems. In this regard, conditions for the attainment of out-of-phase dynamics have received considerable attention, due to the stabilizing effect of asynchrony on global dynamics. At low to moderate rates of dispersal, two coupled subpopulations with intrinsically chaotic dynamics tend to go out-of-phase with one another and also become periodic in their dynamics. The onset of out-of-phase dynamics and periodicity typically coincide. Here, we propose a possible mechanism for the onset of out-of-phase dynamics, and also the stabilization of chaos to periodicity, in two coupled subpopulations with intrinsically chaotic dynamics. We suggest that the onset of out-of-phase dynamics is due to the propensity of chaotic subpopulations governed by a steep, single-humped one-dimensional population growth model to repeatedly reach low subpopulation sizes that are close to a value Nt = A (A ≠ equilibrium population size, K) for which Nt( + 1) = K. Subpopulations with very similar low sizes, but on opposite sides of A, will become out-of-phase in the next generation, as they will end up at sizes on opposite sides of K, resulting in positive growth for one subpopulation and negative growth for the other. The key to the stabilization of out-of-phase periodic dynamics in this mechanism is the net effect of dispersal placing upper and lower bounds to subpopulation size in the two coupled subpopulations, once they have become out-of-phase. We tested various components of this proposed mechanism by simulations using the Ricker model, and the results of the simulations are consistent with predictions from the hypothesized mechanism. Similar results were also obtained using the logistic and Hassell models, and with the Ricker model incorporating the possibility of extinction, suggesting that the proposed mechanism could be key to the attainment and maintenance of out-of-phase periodicity in two-patch metapopulations where each patch has local dynamics governed by a single-humped population growth model.

Effects of symmetric and asymmetric dispersal on the dynamics of heterogeneous metapopulations: two-patch systems revisited.

Although the effects of dispersal on the dynamics of two-patch metapopulations are well studied, potential interactions between local dynamics and asymmetric dispersal remain unexplored. We examined the dynamics of two Ricker models coupled by symmetric or asymmetric constant-fraction dispersal at different rates. Unlike previous studies, we extensively sampled the r1-r2 space and found that stability of the coupled system was markedly affected by interactions between dispersal (in terms of strength and asymmetry) and local dynamics. When both subpopulations were intrinsically chaotic, increased symmetry in the exchange of individuals had a greater stabilizing impact on the dynamics of the system. When one subpopulation showed considerably more unstable dynamics than the other, higher asymmetry in the exchange of individuals had a stabilizing or destabilizing effect on the dynamics depending on whether the net dispersal bias was from the relatively stable to the relatively unstable subpopulation, or vice versa. The sensitivity of chaotic dynamics to stabilization due to dispersal varied with r-value in the chaotic subpopulation. Under unidirectional or bidirectional symmetric dispersal, when one subpopulation was intrinsically chaotic and the other had stable dynamics, the stabilization of chaotic subpopulations with r~3.3-4.0 occurred at the lowest dispersal rates, followed by chaotic subpopulations with r~2.7-2.95 and, finally, chaotic subpopulations with r~2.95-3.3. The mechanism for this pattern is not known but might be related to the range and number of different attainable population sizes possible in different r-value zones.

Effects of constant immigration on the dynamics and persistence of stable and unstable Drosophila populations.

Constant immigration can stabilize population size fluctuations but its effects on extinction remain unexplored. We show that constant immigration significantly reduced extinction in fruitfly populations with relatively stable or unstable dynamics. In unstable populations with oscillations of amplitude around 1.5 times the mean population size, persistence and constancy were unrelated. Low immigration enhanced persistence without affecting constancy whereas high immigration increased constancy without enhancing persistence. In relatively stable populations with erratic fluctuations of amplitude close to the mean population size, both low and high immigration enhanced persistence. In these populations, the amplitude of fluctuations relative to mean population size went down due to immigration, and their dynamics were altered to low-period cycles. The effects of immigration on the population size distribution and intrinsic dynamics of stable versus unstable populations differed considerably, suggesting that the mechanisms by which immigration reduced extinction risk depended on underlying dynamics in complex ways.

Adaptation to larval crowding in Drosophila ananassae leads to the evolution of population stability.

Density-dependent selection is expected to lead to population stability, especially if r and K tradeoff. Yet, there is no empirical evidence of adaptation to crowding leading to the evolution of stability. We show that populations of Drosophila ananassae selected for adaptation to larval crowding have higher K and lower r, and evolve greater stability than controls. We also show that increased population growth rates at high density can enhance stability, even in the absence of a decrease in r, by ensuring that the crowding adapted populations do not fall to very low sizes. We discuss our results in the context of traits known to have diverged between the selected and control populations, and compare our results with previous work on the evolution of stability in D. melanogaster. Overall, our results suggest that density-dependent selection may be an important factor promoting the evolution of relatively stable dynamics in natural populations.