Adaptive Life-history Traits Research Articles

The genetic regulatory architecture and epigenomic basis for age-related changes in rattlesnake venom

Developmental phenotypic changes can evolve under selection imposed by age- and size-related ecological differences. Many of these changes occur through programmed alterations to gene expression patterns, but the molecular mechanisms and gene-regulatory networks underlying these adaptive changes remain poorly understood. Many venomous snakes, including the eastern diamondback rattlesnake (Crotalus adamanteus), undergo correlated changes in diet and venom expression as snakes grow larger with age, providing models for identifying mechanisms of timed expression changes that underlie adaptive life history traits. By combining a highly contiguous, chromosome-level genome assembly with measures of expression, chromatin accessibility, and histone modifications, we identified cis-regulatory elements and trans-regulatory factors controlling venom ontogeny in the venom glands of C. adamanteus. Ontogenetic expression changes were significantly correlated with epigenomic changes within genes, immediately adjacent to genes (e.g., promoters), and more distant from genes (e.g., enhancers). We identified 37 candidate transcription factors (TFs), with the vast majority being up-regulated in adults. The ontogenetic change is largely driven by an increase in the expression of TFs associated with growth signaling, transcriptional activation, and circadian rhythm/biological timing systems in adults with corresponding epigenomic changes near the differentially expressed venom genes. However, both expression activation and repression contributed to the composition of both adult and juvenile venoms, demonstrating the complexity and potential evolvability of gene regulation for this trait. Overall, given that age-based trait variation is common across the tree of life, we provide a framework for understanding gene-regulatory-network-driven life-history evolution more broadly.

Connections to the Deep: Deep Vertical Migrations, an Important Part of the Life Cycle of Apherusa glacialis, an Arctic Ice-Associated Amphipod

Arctic sea ice contains a substantial amount of living biota of which part is lost through melt and export out of the Arctic Ocean every year. It is unclear how populations can be maintained within the Arctic Ocean. A representative ice inhabitant, the amphipodApherusa glacialiswas previously assumed to spend its entire life in the sea ice habitat, hence being dependent on sea ice to complete its life cycle. However, several recent studies report pelagic occurrences and suggest that seasonal vertical migrations might be an adaptive life history trait enabling a viable population size in the Arctic Ocean. In this study we use a particle-tracking model to investigate to what extent vertical migration might affect the species’ retention in the Arctic Ocean and the sea ice habitat. The modeled trajectories ofA. glacialiswere calculated based on ice drift and ocean currents from a coupled ocean – sea ice model covering the Arctic Ocean. We test two scenarios: (1) trajectories ofA. glacialisthat stay attached to the ice or follow the surface currents if they melt out of the ice and (2) trajectories ofA. glacialisthat undertake a seasonal vertical migration to drift with the currents at depth for parts of the year. In the multi-year model simulations it is assumed that after an initial period of 2 yearsA. glacialisthat are located outside sea-ice cover each spring will perish while those located within the ice-covered region will reproduce. The model results show that a seasonal vertical migration both increases the total number of individuals and leads to a population distribution within the Arctic Ocean more in line with previous findings than the results from the non-migratingA. glacialis. Our results support the hypothesis that a seasonal migration may be an adaptive life history strategy in this species.

Zooplankton ecological traits maximize the trophic transfer efficiency of the Humboldt Current upwelling system

Calanid copepods of the genera Calanus and Calanoides are key components of zooplankton communities in upwelling systems. Here, we compare the life-history traits of Calanus chilensis from the Humboldt Current Systems (HCS) off northern Peru and its counterpart Calanoides natalis from the northern Benguela Current System (BCS) off Namibia. A comprehensive data set of the distribution and abundance patterns of these species along extensive horizontal and vertical scales is presented. C. chilensis from the HCS was almost exclusively restricted to the surface layer (50–0 m) above the oxygen minimum zone (OMZ), whereas C. natalis from the BCS inhabited the entire water column down to 800 m performing ontogenetic vertical migration (OVM) through the OMZ. Resting stages of C. natalis at depth accumulated high amounts of lipid (30–60% of dry mass, DM), whereas C. chilensis did not rely on lipid reserves. These findings confirm that the life cycle of C. chilensis does not include OVM with diapause at depth. Surprisingly, the regional distribution of C. chilensis secondary production extended much further offshore (>200 km from the coast) than is typical of other coastal upwelling systems. Deviating environmental conditions forced the two key calanid species to develop specific, but different life strategies for HCS and BCS. Compacted biomass concentrations of C. chilensis in the surface layer from the shelf (≤3 g DM m−2) to offshore waters (≤1.5 g DM m−2) facilitate easy and efficient foraging by predators such as juvenile Peruvian anchovies. In contrast, a large fraction of the C. natalis biomass occurs within the OMZ and is thus out of reach for hypoxia-sensitive predators. Calanoid copepods (e.g. C. chilensis) play a crucial role as important prey for growth and recruitment of small pelagic fish. Thus, the compacted biomass and high productivity of C. chilensis at the surface derived from its adaptive life-history traits (no OVM) may explain the superior trophic transfer efficiency and hence enormous fisheries yield of the HCS compared to the BCS.

Desiccation resistance is an adaptive life-history trait dependent upon cuticular hydrocarbons, and influenced by mating status and temperature in D. melanogaster

Terrestrial insects are susceptible to desiccation and conserve internal water stores by preventing the loss of water due to transpiration across the cuticle. The epicuticle, a thin waxy layer on the outer surface of the insect cuticle is comprised primarily of a complex blend of cuticular hydrocarbons (CHCs) and is integral to preventing cuticular water loss. How the composition of epicuticular lipids (quantity and quality of the specific hydrocarbons) relates to desiccation resistance, however, has been difficult to determine. Here, we establish a model system to test the capacity of CHCs to protect against desiccation in the vinegar fly, Drosophila melanogaster. Using this system, we demonstrate that the oenocytes and CHCs produced by these cells are critically important for desiccation resistance, as measured by survival under desiccative conditions. Additionally, we show that both mating status and developmental temperature influence desiccation resistance. Prior mating increased desiccation survival through the direct transfer of CHCs between sexual partners, as well as through a female-specific response to a male-derived factor transferred during copulation. Together, our results demonstrate that desiccation resistance is an adaptive life-history trait dependent upon CHCs and influenced by prior social interactions and environmental conditions.

A major locus controls local adaptation and adaptive life history variation in a perennial plant

BackgroundThe initiation of growth cessation and dormancy represent critical life-history trade-offs between survival and growth and have important fitness effects in perennial plants. Such adaptive life-history traits often show strong local adaptation along environmental gradients but, despite their importance, the genetic architecture of these traits remains poorly understood.ResultsWe integrate whole genome re-sequencing with environmental and phenotypic data from common garden experiments to investigate the genomic basis of local adaptation across a latitudinal gradient in European aspen (Populus tremula). A single genomic region containing the PtFT2 gene mediates local adaptation in the timing of bud set and explains 65% of the observed genetic variation in bud set. This locus is the likely target of a recent selective sweep that originated right before or during colonization of northern Scandinavia following the last glaciation. Field and greenhouse experiments confirm that variation in PtFT2 gene expression affects the phenotypic variation in bud set that we observe in wild natural populations.ConclusionsOur results reveal a major effect locus that determines the timing of bud set and that has facilitated rapid adaptation to shorter growing seasons and colder climates in European aspen. The discovery of a single locus explaining a substantial fraction of the variation in a key life-history trait is remarkable, given that such traits are generally considered to be highly polygenic. These findings provide a dramatic illustration of how loci of large-effect for adaptive traits can arise and be maintained over large geographical scales in natural populations.

Parallel Evolution of Common Allelic Variants Confers Flowering Diversity in Capsella rubella.

Flowering time is an adaptive life history trait. Capsella rubella, a close relative of Arabidopsis thaliana and a young species, displays extensive variation for flowering time but low standing genetic variation due to an extreme bottleneck event, providing an excellent opportunity to understand how phenotypic diversity can occur with a limited initial gene pool. Here, we demonstrate that common allelic variation and parallel evolution at the FLC locus confer variation in flowering time in C. rubella. We show that two overlapping deletions in the 5' untranslated region (UTR) of C. rubella FLC, which are associated with local changes in chromatin conformation and histone modifications, reduce its expression levels and promote flowering. We further show that these two pervasive variants originated independently in natural C. rubella populations after speciation and spread to an intermediate frequency, suggesting a role of this parallel cis-regulatory change in adaptive evolution. Our results provide an example of how parallel mutations in the same 5' UTR region can shape phenotypic evolution in plants.

Deciphering the adjustment between environment and life history in annuals: lessons from a geographically-explicit approach in Arabidopsis thaliana.

The role that different life-history traits may have in the process of adaptation caused by divergent selection can be assessed by using extensive collections of geographically-explicit populations. This is because adaptive phenotypic variation shifts gradually across space as a result of the geographic patterns of variation in environmental selective pressures. Hence, large-scale experiments are needed to identify relevant adaptive life-history traits as well as their relationships with putative selective agents. We conducted a field experiment with 279 geo-referenced accessions of the annual plant Arabidopsis thaliana collected across a native region of its distribution range, the Iberian Peninsula. We quantified variation in life-history traits throughout the entire life cycle. We built a geographic information system to generate an environmental data set encompassing climate, vegetation and soil data. We analysed the spatial autocorrelation patterns of environmental variables and life-history traits, as well as the relationship between environmental and phenotypic data. Almost all environmental variables were significantly spatially autocorrelated. By contrast, only two life-history traits, seed weight and flowering time, exhibited significant spatial autocorrelation. Flowering time, and to a lower extent seed weight, were the life-history traits with the highest significant correlation coefficients with environmental factors, in particular with annual mean temperature. In general, individual fitness was higher for accessions with more vigorous seed germination, higher recruitment and later flowering times. Variation in flowering time mediated by temperature appears to be the main life-history trait by which A. thaliana adjusts its life history to the varying Iberian environmental conditions. The use of extensive geographically-explicit data sets obtained from field experiments represents a powerful approach to unravel adaptive patterns of variation. In a context of current global warming, geographically-explicit approaches, evaluating the match between organisms and the environments where they live, may contribute to better assess and predict the consequences of global warming.

Intraseasonal Variation in Reproductive Effort: Young Males Finish Last

Age-dependent reproductive timing has been observed in females of a number of species; older females often breed earlier in the season and experience higher reproductive success as a result. However, to date, evidence for within-season variation in reproductive effort (RE) for males has been relatively weak. Males are expected to time RE in light of intraseasonal variations in the availability of receptive females and competition with other males. Young males, which are typically smaller and less experienced, might benefit from breeding later in the season, when male-male competition is less intense. Using a long-term data set of Alpine chamois Rupicapra rupicapra, we sought to evaluate the hypothesis that younger males allocate highest RE late in the breeding season, at a time when older male RE has decreased substantially. Our results support this hypothesis, which suggests that intraseasonal variation in RE may be an adaptive life-history trait for males as well as females.

Adaptation to a seasonally varying environment: a strong latitudinal cline in reproductive diapause combined with high gene flow in Drosophila montana

Adaptation to seasonal changes in the northern hemisphere includes an ability to predict the forthcoming cold season from gradual changes in environmental cues early enough to prepare for the harsh winter conditions. The magnitude and speed of changes in these cues vary between the latitudes, which induces strong selection pressures for local adaptation.We studied adaptation to seasonal changes in Drosophila montana, a northern maltfly, by defining the photoperiodic conditions leading to adult reproductive diapause along a latitudinal cline in Finland and by measuring genetic differentiation and the amount of gene flow between the sampling sites with microsatellites. Our data revealed a clear correlation between the latitude and the critical day length (CDL), in which half of the females of different cline populations enter photoperiodic reproductive diapause. There was no sign of limited gene flow between the cline populations, even though these populations showed isolation by distance. Our results show that local adaptation may occur even in the presence of high gene flow, when selection for locally adaptive life-history traits is strong. A wide range of variation in the CDLs of the fly strains within and between the cline populations may be partly due to gene flow and partly due to the opposing selection pressures for fly reproduction and overwinter survival. This variation in the timing of diapause will enhance populations’ survival over the years that differ in the severity of the winter and in the length of the warm period and may also help them respond to long-term changes in environmental conditions.

Tests for the joint evolution of mating system and drought escape in Mimulus

Self-fertilizing taxa are often found at the range margins of their progenitors, where sub-optimal habitats may select for alternative physiological strategies. The extent to which self-fertilization is favoured directly vs. arising indirectly through correlations with other adaptive life history traits is unclear. Trait responses to selection depend on genetic variation and covariation, as well as phenotypic and genetic responses to altered environmental conditions. We tested predictions of the hypothesis that self-fertilization in Mimulus arises through direct selection on physiological and developmental traits that allow seasonal drought escape. Phenotypic selection on mating system and drought escape traits was estimated in field populations of M. guttatus. In addition, trait phenotype and phenotypic selection were compared between experimental wet and dry soil in two greenhouse populations each of M. guttatus and M. nasutus. Finally, genetic variation and covariation for traits were compared between wet and dry soil treatments in a greenhouse population of M. guttatus. Consistent with predictions, selection for early flowering was generally stronger than for mating system traits, and selection for early flowering was stronger in dry soil. Inconsistent with predictions, selection for water-use efficiency was largely absent; selection for large flowers was stronger than for drought escape in the field; and most drought escape and mating system traits were not genetically correlated. A positive genetic correlation between flowering time and flower size, which opposed the adaptive contour, emerged only in wet soil, suggesting that variation in water availability may maintain variation in these traits. Plastic responses to soil moisture treatments supported the idea that taxonomic divergence could have been facilitated by plasticity in flowering time and selfing. The hypothesis that plant mating systems may evolve indirectly via selection on correlated life history characteristics is plausible and warrants increased attention.

Diaspidid (Hemiptera: Coccoidea) size plasticity as an adaptive life history trait

The size and fecundity of Hemiberlesia lataniae (Signoret) (Hemiptera: Diaspididae) on partially resistant and susceptible kiwifruit (Actinidia spp.) varieties was measured. The size ratio of mature H. lataniae grown on a partially resistant genotype, compared with those on a susceptible genotype, was 0.67-0.51 for 2nd instar exuviae area, 0.32 for adult body area and 0.18 for estimated body volume. The fertility ratio was 0.1, but the pre-oviposition period and the size of the crawlers were the same. Diaspidid scale insects' unusual ability to continue growing after the final moult appears to be a key feature allowing these insects to show extreme size plasticity while retaining the ability to reproduce even when very small. These observations challenge current theories of insect development that postulate the need to achieve a critical weight threshold before the final moult. We suggest that this strategy may have assisted the evolution of polyphagy within the Diaspididae.

Adaptive Diversity: Hormones and Metabolism in Freshwaters

Genes underlying the evolution of morphological traits have recently been identified in a number of model species. In the stickleback, the metabolic adaptations to a freshwater habitat have now been linked to a well-known hormonal system.

Quantifying selection differentials caused by recreational fishing: development of modeling framework and application to reproductive investment in pike (Esox lucius).

Methods for quantifying selection pressures on adaptive traits affected by size-selective fishing are still scarce, and none have as yet been developed for recreational fishing. We present an ecologically realistic age-structured model specifically tailored to recreational fishing that allows estimating selection differentials on adaptive life-history traits. The model accounts for multiple ecological feedbacks, which result in density-dependent and frequency-dependent selection. We study selection differentials on annual reproductive investment under size-selective exploitation in a highly demanded freshwater recreational fish species, northern pike (Esox lucius L.). We find that recreational angling mortality exerts positive selection differentials on annual reproductive investment, in agreement with predictions from life-history theory. The strength of selection increases with the intensity of harvesting. We also find that selection on reproductive investment can be reduced by implementing simple harvest regulations such as minimum-size limits. The general, yet computationally simple, methods introduced here allow evaluating and comparing selection pressures on adaptive traits in other fish populations and species, and thus have the potential to become a tool for evolutionary impact assessment of harvesting.

Living long by staying small: stem layering as an adaptive life-history trait in shade-tolerant tree seedlings

Suppressed seedling banks are important in replacement dynamics in late-successional forests. However, demographic properties of seedling populations are poorly known, and there has been little attention to traits that might affect fitness in suppressed seedlings. Acer saccharum Marsh., a shade-tolerant dominant in eastern North American forests, frequently develops adventitious roots along prostrate portions of stems (“layering”). Measurements of Acer seedlings in old-growth forests in Michigan indicate that layered seedlings proportionally reduce structural allocations to older layered stem tissues, retain leaf area / height ratios of younger unlayered seedlings, and tend to survive longer. In tree seedlings, allometric consequences of normal stem growth lead to declining ratios of photosynthetic to nonphotosynthetic biomass, which potentially reduces shade tolerance and limiting age. The layering habit may defer this penalty by changing the allometry of growth. Resulting increases in life expectancy should increase chance of access to increased light and of reaching the canopy. Thus, because flowering is generally restricted to canopy trees, the tendency to layer may increase fitness. Properties of individuals in suppressed seedling banks may be selectively and ecologically important, shaping life histories and population dynamics.

Reproductive strategy and the compositional dynamics of crustose lichen communities on aspen (Populus tremula L.) in Scotland

Abstract:Ecological studies are essential in understanding the response of crustose lichens to habitat dynamics and developing effective conservation strategy. While the combined response of individual crustose species within a community will be tremendously complex, the overall result of individualistic change can be simplified using trait-based analyses. In this paper we examine the response of crustose species with contrasting reproductive traits (predominantly sexual vs asexual reproduction) and which occur within a closely defined habitat (as epiphytes on the lower bole of aspen) to environmental drivers measured at two different scales, i.e. between and within aspen stands. Our results point to the important effect of tree age and subsequent shifts in bark quality (pH) on the composition of the crustose community. However, shifts in community composition putatively controlled by bark quality comprise a change from a community dominated by sexual species to a community with mostly asexual crusts. Our results suggest therefore that variation within this crustose community may be driven by the combined effects of allogenic change (tree age and bark quality) and autogenic processes that are related to a species’ adaptive life-history traits.

Copepod post-embryonic durations: pattern, conformity, and predictability. The realities of isochronal and equiproportional development, and trends in the opepodid-naupliar duration ratio

A collation of post-embryonic durations for freshwater and marine calanoid, cyclopoid and harpacticoid copepods is provided, and examined for patterns and conformities which may be of predictive value. Most of the analysis concerns calanoids. Only the genus Acartia exhibits evidence of equal stage duration (isochronality). Accordingly, isochronal development must be rejected as a general pattern in copepods — with various implications to the study of their production. Conversely, relative stage durations are surprisingly comparable in a wide range of copepods across a broad range of temperatures and food levels. A loose consistency is evident among copepod species generally, (interspecific equiproportionality), but within given genera, a striking regularity, here termed intergeneric equiproportionality (IGE) is evident. Patterns of IGE are consistent with selectively adaptive life-history traits, and IGE thus offers predictive prospects which are of both quantitative and qualitative (heuristic) value. Empirical support which exists for IGE among marine calanoids suggests that in contrast to isochronality and interspecific equiproportionality, IGE is indeed a real, and ultimately quantifiable feature of copepod development. Within calanoids, the ratio of total copepodid to total naupliar duration (Dc/Dn) appears independent of temperature, shows little relationship to adult body mass, but is inversely related to food supply, markedly so in freshwater forms. In this context, changes in the ratio are attributable largely to influences of food supply upon copepodid development times: naupliar durations appear relatively independent of food concentrations during development. Considerably higher Dc/Dn ratios in freshwater than in marine calanoids conceivably arise from selective influences of different nutritional conditions and size-selective predation pressures in freshwater and marine environments. In the generally high predation environment of freshwaters, acceleration of naupliar development potentially reduces the vulnerability of these smaller stages to size-selective tactile predation, while larger copepodid instars are able to reduce the opposing size-selective influences of visual planktivores by virtue of their escape responses to suction attack. Within the spectrum of copepod life histories and development schedules, ecologically consistent trends of this nature await formal recognition. The present recognition of IGE is a modest initiative in this quest. Both naupliar and copepodid durations are inverse monotonic functions of temperature. Several mathematical expressions which account for this temperature-duration response are provided. The response envelope is much tighter for naupliar than copepodid durations. Predictability of temperature-duration responses accordingly declines ontogenetically from egg to naupliar to copepodid stages.