Evolution Of Timing Research Articles

A rapidly evolved shift in life‐history timing during ecological speciation is driven by the transition between developmental phases

For insect species in temperate environments, seasonal timing is often governed by the regulation of diapause, a complex developmental programme that allows insects to weather unfavourable conditions and synchronize their life cycles with available resources. Diapause development consists of a series of distinct phases including initiation, maintenance, termination and post-diapause development. The evolution of insect seasonal timing depends in part on how these phases of diapause development and post-diapause development interact to affect variation in phenology. Here, we dissect the physiological basis of a recently evolved phenological shift in Rhagoletis pomonella (Diptera: Tephritidae), a model system for ecological divergence. A recently derived population of R.pomonella shifted from specializing on native hawthorn fruit to earlier fruiting introduced apples, resulting in a 3-4week shift in adult emergence timing. We tracked metabolic rates of individual flies across post-winter development to test which phases of development may act either independently or in combination to contribute to this recently evolved divergence in timing. Apple and hawthorn flies differed in a number of facets of their post-winter developmental trajectories. However, divergent adaptation in adult emergence phenology in these flies was due almost entirely to the end of the pupal diapause maintenance phase, with post-diapause development having a very small effect. The relatively simple underpinnings of variation in adult emergence phenology suggest that further adaptation to seasonal change in these flies for this trait might be largely due to the timing of diapause termination unhindered by strong covariance among different components of post-diapause development.

Evolution of contribution timing in public goods games.

Life-history strategies are a crucial aspect of life, which are complicated in group-living species, where pay-offs additionally depend on others' behaviours. Previous theoretical models of public goods games have generally focused on the amounts individuals contribute to the public good. Yet a much less-studied strategic aspect of public goods games, the timing of contributions, can also have dramatic consequences for individual and collective performance. Here, we develop two stage game theoretical models to explore how the timing of contributions evolves. In the first stage, individuals contribute to a threshold public good based on a performance schedule. The second stage begins once the threshold is met, and the individuals then compete as a function of their performance. We show how contributing rapidly is not necessarily optimal, because delayers can act as 'cheats,' avoiding contributing while reaping the benefits of the public good. However, delaying too long can put the delayers at a disadvantage as they may be ill-equipped to compete. These effects lead to bistability in a single group, and spatial diversity among multiple interacting groups.

Adaptive individual variation in phenological responses to perceived predation levels

The adaptive evolution of timing of breeding (a component of phenology) in response to environmental change requires individual variation in phenotypic plasticity for selection to act upon. A major question is what processes generate this variation. Here we apply multi-year manipulations of perceived predation levels (PPL) in an avian predator-prey system, identifying phenotypic plasticity in phenology as a key component of alternative behavioral strategies with equal fitness payoffs. We show that under low-PPL, faster (versus slower) exploring birds breed late (versus early); the pattern is reversed under high-PPL, with breeding synchrony decreasing in conjunction. Timing of breeding affects reproductive success, yet behavioral types have equal fitness. The existence of alternative behavioral strategies thus explains variation in phenology and plasticity in reproductive behavior, which has implications for evolution in response to anthropogenic change.

Earlier migration timing of salmonids: an adaptation to climate change or maladaptation to the fishery?

Recent studies reporting shifts in the timing of salmonid migrations have suggested global warming to be a cause. However, the specific mechanisms underlining the evolution of earlier migration timing in salmonid fishes are unknown. In this paper, I present a hypothesis by which fishery-induced selection works to advance the timing of salmonid migration, given that the timings of migration and breeding are genetically controlled heritable traits. Although late-spawning salmon brood lines enter rivers after early-spawning brood lines, there is evidence that all brood lines arrive in coastal fishing grounds at similar times. As such, late-spawning brood lines would be fished for longer periods of time, with their increased harvest rate imposing directional selection on earlier-spawning brood lines. Thus, fisheries-induced evolution could favor the earlier timing of river entry to escape coastal fisheries. Should earlier migration timing not be an adaptation to global warming — should it be a maladaptation to fisheries-induced selection instead — then it will have a negative impact on the sustainability of salmonid resources.

The genetic architecture underlying diapause termination in a planktonic crustacean.

Diapause is a feature of the life cycle of many invertebrates by which unfavourable environmental conditions can be outlived. The seasonal timing of diapause allows organisms to adapt to seasonal changes in habitat suitability and thus is key to their fitness. In the planktonic crustacean Daphnia, various cues can induce the production of diapause stages that are resistant to heat, drought or freezing and contain one to two embryos in developmental arrest. Daphnia is a keystone species of many freshwater ecosystems, where it acts as the main link between phytoplankton and higher trophic levels. The correct seasonal timing of diapause termination is essential to maintain trophic interactions and is achieved via a genetically based interpretation of environmental cues like photoperiod and temperature. Field monitoring and modelling studies raised concerns on whether populations can advance their seasonal release from diapause to advances in spring phenology under global change, or if a failure to adapt will cause trophic mismatches negatively affecting ecosystem functioning. Our capacity to understand and predict the evolution of diapause timing requires information about the genetic architecture underlying this trait. In this study, we identified eight quantitative trait loci (QTLs) and four epistatic interactions that together explained 66.5% of the variation in diapause termination in Daphnia magna using QTL mapping. Our results suggest that the most significant QTL is modulating diapause termination dependent on photoperiod and is involved in three of the four detected epistatic interactions. Candidate genes at this QTL could be identified through the integration with genome data and included the presynaptic active zone protein bruchpilot. Our findings contribute to understanding the genomic control of seasonal diapause timing in an ecological relevant species.

Keeping time without a spine: what can the insect clock teach us about seasonal adaptation?

Seasonal change in daylength (photoperiod) is widely used by insects to regulate temporal patterns of development and behaviour, including the timing of diapause (dormancy) and migration. Flexibility of the photoperiodic response is critical for rapid shifts to new hosts, survival in the face of global climate change and to reproductive isolation. At the same time, the daily circadian clock is also essential for development, diapause and multiple behaviours, including correct flight orientation during long-distance migration. Although studied for decades, how these two critical biological timing mechanisms are integrated is poorly understood, in part because the core circadian clock genes are all transcription factors or regulators that are able to exert multiple effects throughout the genome. In this chapter, we discuss clocks in the wild from the perspective of diverse insect groups across eco-geographic contexts from the Antarctic to the tropical regions of Earth. Application of the expanding tool box of molecular techniques will lead us to distinguish universal from unique mechanisms underlying the evolution of circadian and photoperiodic timing, and their interaction across taxonomic and ecological contexts represented by insects.This article is part of the themed issue 'Wild clocks: integrating chronobiology and ecology to understand timekeeping in free-living animals'.

Importance of whole-plant biomass allocation and reproductive timing to habitat differentiation across the North American sunflowers.

Trait-based plant ecology attempts to use small numbers of functional traits to predict plant ecological strategies. However, a major gap exists between our understanding of organ-level ecophysiological traits and our understanding of whole-plant fitness and environmental adaptation. In this gap lie whole-plant organizational traits, including those that describe how plant biomass is allocated among organs and the timing of plant reproduction. This study explores the role of whole-plant organizational traits in adaptation to diverse environments in the context of life history, growth form and leaf economic strategy in a well-studied herbaceous system. A phylogenetic comparative approach was used in conjunction with common garden phenotyping to assess the evolution of biomass allocation and reproductive timing across 83 populations of 27 species of the diverse genus Helianthus (the sunflowers). Broad diversity exists among species in both relative biomass allocation and reproductive timing. Early reproduction is strongly associated with resource-acquisitive leaf economic strategy, while biomass allocation is less integrated with either reproductive timing or leaf economics. Both biomass allocation and reproductive timing are strongly related to source site environmental characteristics, including length of the growing season, temperature, precipitation and soil fertility. Herbaceous taxa can adapt to diverse environments in many ways, including modulation of phenology, plant architecture and organ-level ecophysiology. Although leaf economic strategy captures one key aspect of plant physiology, on their own leaf traits are not particularly predictive of ecological strategies in Helianthus outside of the context of growth form, life history and whole-plant organization. These results highlight the importance of including data on whole-plant organization alongside organ-level ecophysiological traits when attempting to bridge the gap between functional traits and plant fitness and environmental adaptation.

Phenotypic plasticity of nest timing in a post-glacial landscape: how do reptiles adapt to seasonal time constraints?

Life histories evolve in response to constraints on the time available for growth and development. Nesting date and its plasticity in response to spring temperature may therefore be important components of fitness in oviparous ectotherms near their northern range limit, as reproducing early provides more time for embryos to complete development before winter. We used data collected over several decades to compare air temperature and nest date plasticity in populations of painted turtles and snapping turtles from a relatively warm environment (southeastern Michigan) near the southern extent of the last glacial maximum to a relatively cool environment (central Ontario) near the northern extent of post-glacial recolonization. For painted turtles, population-level differences in reaction norm elevation for two phenological traits were consistent with adaptation to time constraints, but no differences in reaction norm slopes were observed. For snapping turtle populations, the difference in reaction norm elevation for a single phenological trait was in the opposite direction of what was expected under adaptation to time constraints, and no difference in reaction norm slope was observed. Finally, among-individual variation in individual plasticity for nesting date was detected only in the northern population of snapping turtles, suggesting that reaction norms are less canalized in this northern population. Overall, we observed evidence of phenological adaptation, and possibly maladaptation, to time constraints in long-lived reptiles. Where present, (mal)adaptation occurred by virtue of differences in reaction norm elevation, not reaction norm slope. Glacial history, generation time, and genetic constraint may all play an important role in the evolution of phenological timing and its plasticity in long-lived reptiles.

Evolution in eggs and phases: experimental evolution of fecundity and reproductive timing in Caenorhabditis elegans.

To examine the role of natural selection in fecundity in a variety of Caenorhabditis elegans genetic backgrounds, we used an experimental evolution protocol to evolve 14 distinct genetic strains over 15–20 generations. We were able to generate 790 distinct genealogies, which provided information on both the effects of natural selection and the evolvability of each strain. Among these genotypes are a wild-type (N2) and a collection of mutants with targeted mutations in the daf-c, daf-d and AMPK pathways. Differences are observed in reproductive fitness along with related changes in reproductive timing. The majority of selective effects on fecundity occur during the first few generations of evolution, while the negative selection for reproductive timing occurs on longer time scales. In addition, positive selection on fecundity results in positive and negative strain-dependent selection on reproductive timing. A derivative of population size per generation called reproductive carry-over (RCO) may be informative in terms of developmental selection. While these findings transcend mutations in a specific gene, changes in the RCO measure may nevertheless be products of selection. In conclusion, the broader implications of these findings are discussed, particularly in the context of genotype-fitness maps and the role of uncharacterized mutations in individual variation and evolvability.

An Integrative Endocrine Model for the Evolution of Developmental Timing and Life History of Plethodontids and Other Salamanders

In recent years, many molecular endocrine mechanisms that regulate tissue morphogenesis have been detailed in laboratory amphibian models. However, most of these pathways have not been examined across more closely related species to understand how deviations in endocrine pathways may have contributed to amphibian diversification. The timing of metamorphosis and maturation vary extensively across plethodontid salamanders (including direct developing, biphasic, and paedomorphic species), making them an ideal system for analyzing the evolution of endocrine mechanisms in a phylogenetic context. Recent phylogenetic-based reconstructions concluded that ancestral plethodontids were likely direct developers, and free-living larval periods were independently derived multiple times within this family. Furthermore, within one clade (Spelerpini) there have been multiple independent transitions from biphasic (metamorphic) to paedomorphic developmental modes. This inspires the question: What endocrine/developmental mec...

Integration of Random Forest with population-based outlier analyses provides insight on the genomic basis and evolution of run timing in Chinook salmon (Oncorhynchus tshawytscha).

Anadromous Chinook salmon populations vary in the period of river entry at the initiation of adult freshwater migration, facilitating optimal arrival at natal spawning. Run timing is a polygenic trait that shows evidence of rapid parallel evolution in some lineages, signifying a key role for this phenotype in the ecological divergence between populations. Studying the genetic basis of local adaptation in quantitative traits is often impractical in wild populations. Therefore, we used a novel approach, Random Forest, to detect markers linked to run timing across 14 populations from contrasting environments in the Columbia River and Puget Sound, USA. The approach permits detection of loci of small effect on the phenotype. Divergence between populations at these loci was then examined using both principle component analysis and FST outlier analyses, to determine whether shared genetic changes resulted in similar phenotypes across different lineages. Sequencing of 9107 RAD markers in 414 individuals identified 33 predictor loci explaining 79.2% of trait variance. Discriminant analysis of principal components of the predictors revealed both shared and unique evolutionary pathways in the trait across different lineages, characterized by minor allele frequency changes. However, genome mapping of predictor loci also identified positional overlap with two genomic outlier regions, consistent with selection on loci of large effect. Therefore, the results suggest selective sweeps on few loci and minor changes in loci that were detected by this study. Use of a polygenic framework has provided initial insight into how divergence in a trait has occurred in the wild.

Species Introductions and Their Cascading Impacts on Biotic Interactions in desert riparian ecosystems.

Desert riparian ecosystems of North America are hotspots of biodiversity that support many sensitive species, and are in a region experiencing some of the highest rates of climatic alteration in North America. Fremont cottonwood, Populus fremontii, is a foundation tree species of this critical habitat, but it is threatened by global warming and regional drying, and by a non-native tree/shrub, Tamarix spp., all of which can disrupt the mutualism between P. fremontii and its beneficial mycorrhizal fungal communities. Specialist herbivorous leaf beetles (Diorhabda spp.) introduced for biocontrol of Tamarix are altering the relationship between this shrub and its environment. Repeated episodic feeding on Tamarix foliage by Diorhabda results in varying rates of dieback and mortality, depending on genetic variation in allocation of resources, growing conditions, and phenological synchrony between herbivore and host plant. In this article, we review the complex interaction between climatic change and species introductions and their combined impacts on P. fremontii and their associated communities. We anticipate that (1) certain genotypes of P. fremontii will respond more favorably to the presence of Tamarix and to climatic change due to varying selection pressures to cope with competition and stress; (2) the ongoing evolution of Diorhabda's life cycle timing will continue to facilitate its expansion in North America, and will over time enhance herbivore impact to Tamarix; (3) defoliation by Diorhabda will reduce the negative impact of Tamarix on P. fremontii associations with mycorrhizal fungi; and (4) spatial variability in climate and climatic change will modify the capacity for Tamarix to survive episodic defoliation by Diorhabda, thereby altering the relationship between Tamarix and P. fremontii, and its associated mycorrhizal fungal communities. Given the complex biotic/abiotic interactions outlined in this review, conservation biologists and riparian ecosystem managers should strive to identify and conserve the phenotypic traits that underpin tolerance and resistance to stressors such as climate change and species invasion. Such efforts will greatly enhance conservation restoration efficacy for protecting P. fremontii forests and their associated communities.

Adaptation of timing of life history traits and population dynamic responses to climate change in spatially structured populations

Changes in the seasonal timing of life history events are documented effects of climate change. We used a general model to study how dispersal and competitive interactions affect eco-evolutionary responses to changes in the temporal distribution of resources over the season. Specifically, we modeled adaptation of the timing of reproduction and population dynamic responses in two competing populations that disperse between two habitats characterized by an early and late resource peak. We investigated three scenarios of environmental change: (1) food peaks advance in both habitats, (2) in the late habitat only and (3) in the early habitat only. At low dispersal rates the evolutionarily stable timing of reproduction closely matched the local resource peak and the environmental change typically caused population decline. Larger dispersal rates rendered less intuitive eco-evolutionary population responses. First, dispersal caused mismatch between evolutionarily stable timing of reproduction and local resource peaks and as a result, reproductive output for subpopulations could increase as well as decrease when resource availability underwent temporal shifts. Second, population responses were contingent on competition between populations. This could accelerate population declines and cause extinctions or even reverse population trends from negative to positive compared to the low dispersal case. When dispersal rate was large and the early resource peak was advanced available niche space was reduced. Hence, even when a population survived the environmental change and obtained positive equilibrium population density, subsequent adaptation of competing populations could drive it to extinction due to convergent evolution and competitive exclusion. These results shed new light on the role of competition and dispersal for the evolution of timing of life history events and provide guidelines for understanding short and long-term population response to climate change.

Timing of seed germination correlated with temperature-based environmental conditions during seed development in conifers

Ecological (climatic and geographic) variation in early life-history transitions is a vital determinant of the adaptive evolution of timing of seed germination. This study aimed to investigate the correlation between timing of seed germination and environmental conditions during seed development. We examined seed germination timing of 15 coniferous seed lots of lodgepole pine, ‘interior’ spruce and western hemlock collected from natural stands in British Columbia (BC), Canada, under manipulated [stratification, thermo-priming (15 or 20°C) and their combinations] and non-manipulated (control) conditions. Timing of seed germination showed strong and positive correlation with the temperature-based environmental condition during seed development. This pattern persisted across species and seed lots within species, substantiating the historic importance of environmental conditions during seed development and maturation to life-history traits. Moreover, the strategy of phenotypic plasticity affecting timing of seed germination was observed across the applied germination treatments. These results provide insight into the germination niche as affected by global warming, indicating that conifers' seed dormancy in BC (north of 54°N) tends to increase and the changes associated with early spring warm-up are expected to accelerate seedling emergence, as shortened winters would have a minimal effect on dormancy decay.

Does the temporal mismatch hypothesis match in boreal populations?

The temporal mismatch hypothesis suggests that fitness is related to the degree of temporal synchrony between the energetic needs of the offspring and their food supply. The hypothesis has been a basis in studying the influence of climate warming on nature. This study enhances the knowledge on prevalence of temporal mismatches and their consequences in boreal populations, and questions the role of the temporal mismatch hypothesis as the principal explanation for the evolution of timing of breeding. To test this, we examined if synchrony with caterpillar prey or timing of breeding per se better explains reproductive output in North European parid populations. We compared responses of temperate-origin species, the great tit (Parus major) and the blue tit (Cyanistes caeruleus), and a boreal species, the willow tit (Poecile montanus). We found that phenologies of caterpillars and great tits, but not of blue tits, have advanced during the past decades. Phenologies correlated with spring temperatures that may function as cues about the timing of the food peak for great and blue tits. The breeding of great and blue tits and their caterpillar food remained synchronous. Synchrony explained breeding success better than timing of breeding alone. However, the synchrony effect arose only in certain conditions, such as with high caterpillar abundances or high breeding densities. Breeding before good synchrony seems advantageous at high latitudes, especially in the willow tit. Thus, the temporal mismatch hypothesis appears insufficient in explaining the evolution of timing of breeding.

Clock gene evolution: seasonal timing, phylogenetic signal, or functional constraint?

Genetic determinants of seasonal reproduction are not fully understood but may be important predictors of organism responses to climate change. We used a comparative approach to study the evolution of seasonal timing within a fish community in a natural common garden setting. We tested the hypothesis that allelic length variation in the PolyQ domain of a circadian rhythm gene, Clock1a, corresponded to interspecific differences in seasonal reproductive timing across 5 native and 1 introduced cyprinid fishes (n = 425 individuals) that co-occur in the Rio Grande, NM, USA. Most common allele lengths were longer in native species that initiated reproduction earlier (Spearman's r = -0.70, P = 0.23). Clock1a allele length exhibited strong phylogenetic signal and earlier spawners were evolutionarily derived. Aside from length variation in Clock1a, all other amino acids were identical across native species, suggesting functional constraint over evolutionary time. Interestingly, the endangered Rio Grande silvery minnow (Hybognathus amarus) exhibited less allelic variation in Clock1a and observed heterozygosity was 2- to 6-fold lower than the 5 other (nonimperiled) species. Reduced genetic variation in this functionally important gene may impede this species' capacity to respond to ongoing environmental change.

One phase of the dormancy developmental pathway is critical for the evolution of insect seasonality

Evolutionary change in the timing of dormancy enables animals and plants to adapt to changing seasonal environments and can result in ecological speciation. Despite its clear biological importance, the mechanisms underlying the evolution of dormancy timing in animals remain poorly understood because of a lack of anatomical landmarks to discern which phase of dormancy an individual is experiencing. Taking advantage of the nearly universal characteristic of metabolic suppression during insect dormancy (diapause), we use patterns of respiratory metabolism to document physiological landmarks of dormancy and test which of the distinct phases of the dormancy developmental pathway contribute to a month-long shift in diapause timing between a pair of incipient moth species. Here, we show that divergence in life cycle between the earlier-emerging E-strain and the later-emerging Z-strain of European corn borer (ECB) is clearly explained by a delay in the timing of the developmental transition from the diapause maintenance phase to the termination phase. Along with recent findings indicating that life-cycle differences between ECB strains stem from allelic variation at a single sex-linked locus, our results demonstrate how dramatic shifts in animal seasonality can result from simple developmental and genetic changes. Although characterizing the multiple phases of the diapause developmental programme in other locally adapted populations and species will undoubtedly yield surprises about the nature of animal dormancy, results in the ECB moth suggest that focusing on genetic variation in the timing of the dormancy termination phase may help explain how (or whether) organisms rapidly respond to global climate change, expand their ranges after accidental or managed introductions, undergo seasonal adaptation, or evolve into distinct species through allochronic isolation.

Behavioral plasticity mitigates risk across environments and predators during anuran metamorphosis

Most animals metamorphose, changing morphology, physiology, behavior and ecological interactions. Size- and habitat-dependent mortality risk is thought to affect the evolution and plastic expression of metamorphic timing, and high predation during the morphological transition is posited as a critical selective force shaping complex life cycles. Nonetheless, empirical data on how risk changes across metamorphosis and stage-specific habitats, or how that varies with size, are rare. We examined predator-prey interactions of red-eyed treefrogs, Agalychnis callidryas, with an aquatic predator (giant water bug, Belostoma) and a semi-terrestrial predator (fishing spider, Thaumasia) across metamorphosis. We manipulated tadpole density to generate variation in metamorph size and conducted predation trials at multiple developmental stages. We quantified how frog behavior (activity) changes across metamorphic development, habitats, and predator presence or absence. In aquatic trials with water bugs, frog mortality increased with forelimb emergence, as hypothesized. In semi-terrestrial trials, contrary to predictions, predation by spiders increased, not decreased, with tail resorption. In neither case did frog size affect mortality. Frogs reduced activity upon forelimb emergence in the water, and further with emergence into air, then increased activity with tail resorption. Longer-tailed metamorphs were captured more often in spider attacks, but attacked less, as most attacks followed prey movements. Metamorphs behaviorally compensated for poor escape performance more effectively on land than in water, thus emergence timing may critically affect mortality. The developmental timing of the ecological transition between environments that select for different larval and juvenile phenotypes is an important, neglected variable in studies of complex life cycles.

The Evolution of Strategic Timing in Collective-Risk Dilemmas

In collective-risk dilemmas, a group needs to collaborate over time to avoid a catastrophic event. This gives rise to a coordination game with many equilibria, including equilibria where no one contributes, and thus no measures against the catastrophe are taken. In this game, the timing of contributions becomes a strategic variable that allows individuals to interact and influence one another. Herein, we use evolutionary game theory to study the impact of strategic timing on equilibrium selection. Depending on the risk of catastrophe, we identify three characteristic regimes. For low risks, defection is the only equilibrium, whereas high risks promote equilibria with sufficient contributions. Intermediate risks pose the biggest challenge for cooperation. In this risk regime, the option to interact over time is critical; if individuals can contribute over several rounds, then the group has a higher chance to succeed, and the expected welfare increases. This positive effect of timing is of particular importance in larger groups, where successful coordination becomes increasingly difficult.

Risk‐induced hatching timing shows low heritability and evolves independently of spontaneous hatching in red‐eyed treefrogs

Plasticity in the timing of transitions between stages of complex life cycles allows organisms to adjust their growth and development to local environmental conditions. Genetic variation in such plasticity is common, but the evolution of context-dependent transition timing may be constrained by information reliability, lag-time and developmental constraints. We studied the genetic architecture of hatching plasticity in embryos of the red-eyed treefrog (Agalychnis callidryas) in response to simulated predator attacks using a series of paternal and maternal half-sibs from a captive breeding colony of wild-collected animals. We compared the developmental timing of induced early hatching across sibships and estimated cross-environment genetic correlations between induced and spontaneous hatching traits. Additive genetic variance for induced early hatching was very low, indicating a constraint on the short-term evolution of earlier hatching timing. This constraint is likely related to the maturation of the hatching mechanism. The most plastic genotypes produced the most extreme spontaneous hatching phenotypes, indicating that developmental range, per se, is not constrained. Cross-environment genetic correlation in hatching timing was negligible, so the evolution of spontaneous hatching in this species has not depended on the evolution of risk-induced hatching and vice versa.