Niche-driven evolution of metabolic and life-history strategies in natural and domesticated populations of Saccharomyces cerevisiae

Background  

Variation of resource supply is one of the key factors that drive the evolution of life-history strategies, and hence the interactions between individuals. In the yeast Saccharomyces cerevisiae, two life-history strategies related to different resource utilization have been previously described in strains from different industrial origins. In this work, we analyzed metabolic traits and life-history strategies in a broader collection of yeast strains sampled in various ecological niches (forest, human body, fruits, laboratory and industrial environments).     

Comparative Life Histories and Ecophysiology of Drosophila melanogaster and D. simulans

Numerous laboratory investigations have compared Drosophila melanogaster and D. simulans for various life history traits and fitness related ecophysiological parameters. From presently available information, it is however difficult to get a general comparative pattern describing the divergence of their ecological niches and understanding their demographic success. Two environmental factors seem however to have played a major role: temperature and alcoholic resources. From an ecophysiological approach, D. simulans may be described as generally more sensitive to stresses; other results point to this species as more cold adapted than its sibling; in some cases, however, D. simulans may appear as better adapted to a warm environment. When investigated, ecophysiological traits show a lesser geographic variability in D. simulans than in D. melanogaster. Presently available information does not explain the ecological prevalence of D. simulans in many places with a mild temperate or subtropical climate. This is presumably due to the fact that most comparisons have been done at a single, standard temperature of 25 degrees C. Comparative studies should be undertaken, spanning the thermal ranges of the two species, and the phenotypic plasticity of ecophysiological traits should now be considered.     

"Ant" and "grasshopper" life-history strategies in Saccharomyces cerevisiae

From the evolutionary and ecological points of view, it is essential to distinguish between the genetic and environmental components of the variability of life-history traits and of their trade-offs. Among the factors affecting this variability, the resource uptake rate deserves particular attention, because it depends on both the environment and the genetic background of the individuals. In order to unravel the bases of the life-history strategies in yeast, we grew a collection of twelve strains of Saccharomyces cerevisiae from different industrial and geographical origins in three culture media differing for their glucose content. Using a population dynamics model to fit the change of population size over time, we estimated the intrinsic growth rate (r), the carrying capacity (K), the mean cell size and the glucose consumption rate per cell. The life-history traits, as well as the glucose consumption rate, displayed large genetic and plastic variability and genetic-by-environment interactions. Within each medium, growth rate and carrying capacity were not correlated, but a marked trade-off between these traits was observed over the media, with high K and low r in the glucose rich medium and low K and high r in the other media. The cell size was tightly negatively correlated to carrying capacity in all conditions. The resource consumption rate appeared to be a clear-cut determinant of both the carrying capacity and the cell size in all media, since it accounted for 37% to 84% of the variation of those traits. In a given medium, the strains that consume glucose at high rate have large cell size and low carrying capacity, while the strains that consume glucose at low rate have small cell size but high carrying capacity. These two contrasted behaviors may be metaphorically defined as "ant" and "grasshopper" strategies of resource utilization. Interestingly, a strain may be "ant" in one medium and "grasshopper" in another. These life-history strategies are discussed with regards to yeast physiology, and in an evolutionary perspective.     

Trait‐based life strategies,ecological niches,and niche overlap in the nekton of the data‐poor Mediterranean Sea

Biological traits can determine species ecological niches and define species responses to environmental variation. Species have a specific functional position in the biological community, resulting in interactions like interspecific competition. In this study, we used biological traits in order to define the life strategies of 205 nektonic species of the Mediterranean Sea. Furthermore, traits related to resource use were analyzed to determine the level of trait and niche overlap and their relationship to life strategies. Focusing on habitats of importance (Posidonia beds, coralligène formations, and lagoons), we investigated strategies and niches of the species present there. Finally, we examined the life strategy of Lessepsian species and investigated the niche overlap between them and indigenous species. Archetypal analysis indicated the existence of three life histories corresponding to strategies already documented for fish (equilibrium, periodic, and opportunistic), with some species also placed in intermediate positions. Niche overlap was evaluated by multiple correspondence analysis and the generation of a single distance metric between all species pairs. This identified species occupying relatively empty (underexploited) ecological niches, like the Lessepsian species Siganus luridus and S. rivulatus, a finding that can also be associated with their establishment in the Mediterranean. Most Lessepsian species were associated with the opportunistic life history strategy, again an important aspect related to their establishment. Also, we documented that most species occurring in important habitats have a relatively high overlap of niches. No significant differences were found in the life strategies across Mediterranean habitats; however, variation in niche overlap and traits related to habitat use was detected. The findings can be useful to determine theoretical competition between species and to identify empty ecological niches. Fisheries science can also benefit from comprehending the dynamics of competing stocks or predict the responses of data‐poor stocks to anthropogenic stressors from known examples of species with shared life strategies.     

Traits of butterfly communities change from specialist to generalist characteristics with increasing land-use intensity

Land-use intensification leads to species loss and shifts in community composition, but only few studies examine how these dynamics affect ecological and life-history traits. We thus investigated whether ecological and life-history traits differ between butterfly communities of grasslands with different land-use intensity. We conducted butterfly transect surveys in 137 grassland sites in three regions of Germany and compiled 10 species-specific ecological and life-history traits from the literature. These traits are associated with food plant specialisation, dispersal, distribution, reproduction and development. We calculated a land-use intensity gradient based on the amount of fertilise mowing frequency and grazing intensity. We analysed differences of traits characteristics between butterfly communities along the land-use intensity gradient in a fourth-corner analysis, thus considering correlations between traits. Six ecological and life-history traits changed from characteristics associated with specialists to such associated with generalists with increasing land-use intensity. These traits characteristics in intensified grasslands were: high dispersal propensity, large distribution range, low population density, more than one generation per year, hibernation in a more advanced developmental stage and a long flight period. The functional homogenisation of the butterfly communities with changes from specialist to generalist trait characteristics with increasing land-use intensity may have severe consequences for ecosystem functioning and services.     

Local adaptation in rotifer populations

The adaptation of organisms to their environment has been a subject of study for a long time. One method to study adaptations in populations involves comparing contemporary populations of the same species under different selective regimes, in what is known as a ??local adaptation?? study. A previous study of the cyclically parthenogenetic rotifer Brachionus plicatilis found high heritabilities for some life-history traits. Some of these life-history traits significantly differed among six populations from Eastern Spain and data suggested some traits to have higher evolutionary rates than neutral genetic markers. Here, by studying the same B. plicatilis populations, we examine the variation and possible local adaptation of their main life-history traits, closely related to fitness, in relation to habitat salinity and temperature. These environmental factors have been shown to play a key role in the ecological differentiation among co-generic species of B. plicatilis. The results obtained in this study show that: (1) the seasonality of rotifer populations from Eastern Spain has profoundly influenced sexual reproduction strategies; (2) salinity is probably a key factor in the ecological specialization of some populations; and (3) rotifer populations harbour high variability in their fitness components.     

Contrasting life history strategies of sympatric Arctic charr morphs, Salvelinus alpinus

In polymorphic populations morphs usually diverge in morphology, ecology and life history, which is most likely driven by adaptations to different environments or resources. Sympatric morphs may develop differences in several life history traits to be able to maximize fitness in alternative niches and habitats. Here, the contrasting life history traits of three sympatric Arctic charr (Salvelinus alpinus (L.)) morphs in a deep and oligotrophic lake in sub-arctic Norway are addressed. The charr morphs differ in spawning habitat and trophic niche. One is a littoral spawning morph that feeds on benthic invertebrates and zooplankton in the littoral and pelagic zones (referred to as the LO-morph), and two other are profundal spawning morphs that either utilize profundal soft bottom benthos as food resource (the PB-morph) or are piscivorous (the PP-morph). The LO-morph typically had intermediate life-history traits relative to the two profundal morphs that had highly contrasting life history traits, especially in growth and age and size of maturity. The PB-morph matured at a young age (～3 years) and at a small body size (～8.5 cm), thereby increasing their fitness by investing in reproduction early in life, which results in a short generation time and decreased probability of being predated before first reproduction. The PP-morph on the other hand, matured at an old age (～9.2 years) and a large body size (～26 cm), thereby increasing their fitness by investing in somatic growth to enhance initial fecundity, and also to reach a large body size profitable for piscivory. The different trade-off regime between the PP- and PB-morphs seems to be caused by adaptation to alternative trophic niches, and appears to be an important factor for the co-occurrence of the two sister-morphs in the profundal zone.     

Life-history phenotypes in a live-bearing fish Brachyrhaphis episcopi living under different predator regimes: seasonal effects?

Several key life-history attributes in a tropical live-bearing fish, Brachyrhaphis episcopi, have previously been shown to differ between populations that co-occur with large predatory fish (Characin sites) and those that do not (Rivulus sites). Here we show that differences between Characin and Rivulus localities are also repeatable over time; patterns observed in the wet season also persisted during the dry. Both sexes reached maturity at a smaller size at Characin sites. Although there was no difference in fecundity between larger females living in different predator communities, smaller females at Characin sites produced more offspring. Females also produced smaller offspring at Characin localities. These differences are remarkably similar to those reported in two other species of live-bearing fish, B. rhabdophora and Poecilia reticulata suggesting possible convergent adaptation in life-history strategies due to predator-mediated effects or correlates thereof. We also found seasonal changes in life-history traits that were independent of predator community. In the wet season, mature males were larger, females allocated more to reproduction, and offspring mass was also greater. The results of our study generate testable predictions using B. episcopi to further our understanding of life-history evolution.     

Differences in dispersal- and colonization-related traits between taxa from the freshwater and the terrestrial realm

The aquatic and terrestrial realms differ in many physical properties that not only require specific physiological adaptations but also cause differences in dispersal options. We thus expect that life-history traits related to dispersal and colonization are under selection pressure because freshwater habitats are more isolated and thus more difficult to reach. We compared traits from European databases of three taxonomic groups along the passive–active dispersal gradient: plants (Plantes), snails (Mollusca: Gastropoda: Prosobranchia et Pulmonata) and hoverflies (Diptera: Syrphidae), all of which have both terrestrial and freshwater species (plants and snails) or early life stages (hoverflies). Aquatic taxa seem to be more successful long-distance dispersers than are terrestrial taxa. Our analysis also revealed lower numbers of seeds or eggs produced in the aquatic habitats. However, aquatic taxa often allocate resources to offspring guarding (vegetative propagules in plants, egg capsules in snails) and breeding-site selection (syrphids). Colonization of the aquatic realm is reinforced by increases in life span (plants), clonal spread (plants), shorter generation times (snails), selfing ability (marginal effect in pulmonate snails) or paedogenesis (two incidences in hoverflies, needs further studies). Probably, the variety of strategies reflects the different evolutionary backgrounds that elicit different combinations of trade-offs, but all traits also might increase invasibility of species.     

Seasonality and the scheduling of life history at different latitudes

For many ectotherms, the annual cycle is partitioned into 'growing' (summer) and 'non-growing' (winter) seasons, and the lengths of these seasons are inversely related across a latitudinal gradient. This pattern of variation has the potential to affect diverse life-history traits profoundly. A key selective agent is size-dependent winter mortality which, with increasing latitude, places an increasing premium on attainment of large body size before the first winter of life. Winter body size is determined primarily by two factors: (1) birth date, which defines the beginning of the first growing season and (2) somatic growth rate within the first season. Using examples drawn from the Atlantic silverside, Menidia menidia (L.), and other fishes, I show how latitudinal variation in the scheduling of the spawning season, countergradient variation in the capacity for growth and reproduction, and mode of sex determination (environmental v. genetic) represent adaptations to seasonality.     

Phenotypic plasticity allows the Mediterranean parsley frog Pelodytes punctatus to exploit two temporal niches under continuous gene flow

Environmental changes, such as climate change, lead to the opening of new niches. In such situations, species that adapt to new niches can survive and/or expand their ranges. However, gene flow can hamper genetic adaptation to new environments. Alternatively, recent models have highlighted the importance of phenotypic plasticity in tracking environmental change. Here, we investigate whether phenotypic plasticity or genetic evolution (or both) allows an amphibian species to exploit two divergent climatic niches. In the Mediterranean region, the parsley frog Pelodytes punctatus breeds both in spring, as do most other species, and in autumn, a temporal niche not exploited by most other species, but which may become increasingly important with global warming. Conditions of development are dramatically different between the two seasons and deeply impact tadpole life-history traits. To determine whether these temporal niches are exploited by two genetically differentiated subpopulations, or whether the bimodal phenology arises in a panmictic population displaying plastic life-history traits, we use two complementary approaches. We measure both molecular genetic differentiation and quantitative-trait differentiation between spring and autumn cohorts, using microsatellites and common garden experiments, respectively. Seasonal cohorts were not genetically differentiated and differences in tadpole life history between cohorts were not maintained in laboratory conditions. We conclude that phenotypic plasticity, rather than genetic adaptation, allows Parsley frog to exploit two contrasting temporal niches.     

Eutrophication and fragmentation are related to species’ rate of decline but not to species rarity: results from a functional approach

Due to ubiquitous eutrophication and fragmentation, many plant species are actually threatened in Europe. Most ecosystems face an overall nutrient input leading to changes in species composition. Fragmentation is effectively influencing species survival. We investigate if two different measures of species performance of 91 calcareous grassland species–rate of decline and rarity—are related to comparable traits and hence processes. On the one hand we expected that species rate of decline is mainly determined by the processes of eutrophication and fragmentation. On the other hand we hypothesized that the importance of site characteristics may overwhelm the effect of eutrophication and fragmentation for species rarity. Hence, we compared persistence traits responding to eutrophication, dispersal traits being related to fragmentation and ecological site factors for decreasing and increasing species and for rare and common species. The results suggest that increasing species had better means of long-distance dispersal and were more competitive than decreasing species. In contrast, there were hardly any differences in traits between rare and common species, but site characteristics were related to species rarity. Rare species were in the main those with ecological preferences for warm, dry, light and nutrient poor conditions. This study may represent a basis for the assessment of plant species threat. Applying the deduced knowledge about the life history of decreasing versus increasing species to habitat-scale approaches it is possible to predict which species may become threatened in the future simply from the combination of their trait values. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Effect of Domestication on the Spread of the [PIN+] Prion in Saccharomyces cerevisiae

Prions (infectious proteins) cause fatal neurodegenerative diseases in mammals. In the yeast Saccharomyces cerevisiae, many toxic and lethal variants of the [PSI+] and [URE3] prions have been identified in laboratory strains, although some commonly studied variants do not seem to impair cell growth. Phylogenetic analysis has revealed four major clades of S. cerevisiae that share histories of two prion proteins and largely correspond to different ecological niches of yeast. The [PIN+] prion was most prevalent in commercialized niches, infrequent among wine/vineyard strains, and not observed in ancestral isolates. As previously reported, the [PSI+] and [URE3] prions are not found in any of these strains. Patterns of heterozygosity revealed genetic mosaicism and indicated extensive outcrossing among divergent strains in commercialized environments. In contrast, ancestral isolates were all homozygous and wine/vineyard strains were closely related to each other and largely homozygous. Cellular growth patterns were highly variable within and among clades, although ancestral isolates were the most efficient sporulators and domesticated strains showed greater tendencies for flocculation. [PIN+]-infected strains had a significantly higher likelihood of polyploidy, showed a higher propensity for flocculation compared to uninfected strains, and had higher sporulation efficiencies compared to domesticated, uninfected strains. Extensive phenotypic variability among strains from different environments suggests that S. cerevisiae is a niche generalist and that most wild strains are able to switch from asexual to sexual and from unicellular to multicellular growth in response to environmental conditions. Our data suggest that outbreeding and multicellular growth patterns adapted for domesticated environments are ecological risk factors for the [PIN+] prion in wild yeast.     

Geographic distributions shape the functional traits in a large mammalian family

Traits of organisms are shaped by their living environments and also determined in part by their phylogenetic relationships. For example, phylogenetic relationships often affect the geographic distributions of animals and cause variation in their living environments, which usually play key roles in the life history and determine the functional traits of species. As an ancient family of mammals, bears widely distribute and have evolved some specific strategies for survival and reproduction during their long‐term evolutionary histories. Many studies on the ecology of bears have been conducted in recent decades, but few have focused on the relationships between their geographic distributions and ecological adaptations. Here, using bears as a model system, we collected and reanalyzed data from the available literatures to explore how geographic distributions and phylogenetic relationships shape the functional traits of animals. We found a positive relationship between phylogenetic relatedness and geographic distributions, with bears distributed in adjacent areas applying more similar strategies to survive and reproduce: (a) Bears living at high latitudes consumed a higher proportion of vertebrates, which may provide more fat for adaptation to low temperatures, and (b) their reproduction rhythms follow fluctuations in seasonal forage availability and quality, in which bears reach mating status from March to May and give birth in approximately November or later.     

Phenotypic landscape of Saccharomyces cerevisiae during wine fermentation: evidence for origin-dependent metabolic traits

The species Saccharomyces cerevisiae includes natural strains, clinical isolates, and a large number of strains used in human activities. The aim of this work was to investigate how the adaptation to a broad range of ecological niches may have selectively shaped the yeast metabolic network to generate specific phenotypes. Using 72 S. cerevisiae strains collected from various sources, we provide, for the first time, a population-scale picture of the fermentative metabolic traits found in the S. cerevisiae species under wine making conditions. Considerable phenotypic variation was found suggesting that this yeast employs diverse metabolic strategies to face environmental constraints. Several groups of strains can be distinguished from the entire population on the basis of specific traits. Strains accustomed to growing in the presence of high sugar concentrations, such as wine yeasts and strains obtained from fruits, were able to achieve fermentation, whereas natural yeasts isolated from "poor-sugar" environments, such as oak trees or plants, were not. Commercial wine yeasts clearly appeared as a subset of vineyard isolates, and were mainly differentiated by their fermentative performances as well as their low acetate production. Overall, the emergence of the origin-dependent properties of the strains provides evidence for a phenotypic evolution driven by environmental constraints and/or human selection within S. cerevisiae.     

Effects of dietary protein:carbohydrate balance on life-history traits in six laboratory strains of Drosophila melanogaster

Drosophila melanogaster Meigen (Diptera: Drosophilidae) is a key model insect for studying life span and aging. Many laboratory strains of D. melanogaster are currently used by laboratories worldwide, but they are known to vary considerably in their physiology, behavior, and life histories. Although the importance of dietary protein:carbohydrate (P:C) balance as a predominant determinant of life span and other life-history traits has been highlighted in recent research, it remains unexplored whether the impacts of P:C balance on these fitness-related traits vary in a strain-specific manner in D. melanogaster. In this study, we compared the life-history consequences (life span, egg production rate, pre-adult survival, development time, and body mass at eclosion) of six laboratory strains of D. melanogaster (w1118, yw, Oregon-R, white Canton-S, Canton-S-SNU, and Canton-S-Inha) allocated to one of four synthetic diets differing in P:C ratio (1:16, 1:4, 1:1, or 4:1). The effects of dietary P:C balance on various adult and larval life-history traits were qualitatively similar across all strains studied in this study. Regardless of fly strain, adults exhibited a shortened life span and improved egg production on a diet with the highest P:C ratio of 4:1. In all strains, larvae raised on a diet comprising the lowest P:C ratio of 1:16 suffered high mortality, delayed development time, and reduced body mass. Despite the general similarity in the direction of the effect of P:C balance across strains, fly strains differed in the magnitude of their life-history responses to dietary P:C balance, as indicated by a significant interaction between fly strain and dietary P:C ratio for all measured traits except body mass at eclosion. Possible mechanisms explaining such strain-specific responses are discussed.     

Putting phylogeny into the analysis of biological traits: A methodological approach

Phylogenetic comparative methods have long considered phylogenetic signal as a source of statistical bias in the correlative analysis of biological traits. However, the main life-history strategies existing in a set of taxa are often combinations of life history traits that are inherently phylogenetically structured. In this paper, we present a method for identifying evolutionary strategies from large sets of biological traits, using phylogeny as a source of meaningful historical and ecological information. Our methodology extends a multivariate method developed for the analysis of spatial patterns, and relies on finding combinations of traits that are phylogenetically autocorrelated. Using extensive simulations, we show that our method efficiently uncovers phylogenetic structures with respect to various tree topologies, and remains powerful in cases where a large majority of traits are not phylogenetically structured. Our methodology is illustrated using empirical data, and implemented in the adephylo package for the free software R.     

Methylation patterns of Tf2 retrotransposons linked to rapid adaptive stress response in the brown planthopper (Nilaparvata lugens)

Transposable elements (TEs) exhibit vast diversity across insect orders and are one of the major factors driving insect evolution and speciation. Presence of TEs can be both beneficial and deleterious to their host. While it is well-established that TEs impact life-history traits, adaptations and survivability of insects under hostile environments, the influence of the ecological niche on TE-landscape remains unclear. Here, we analysed the dynamics of Tf2 retrotransposons in the brown planthopper (BPH), under environmental fluctuations. BPH, a major pest of rice, is found in almost all rice-growing ecosystems. We believe genome plasticity, attributed to TEs, has allowed BPH to adapt and colonise novel ecological niches. Our study revealed bimodal age-distribution for Tf2 elements in BPH, indicating the occurrence of two major transpositional events in its evolutionary history and their contribution in shaping BPH genome. While TEs can provide genome flexibility and facilitate adaptations, they impose massive load on the genome. Hence, we investigated the involvement of methylation in modulating transposition in BPH. We performed comparative analyses of the methylation patterns of Tf2 elements in BPH feeding on resistant- and susceptible-rice varieties, and also under pesticide stress, across different life-stages. Results confirmed that methylation, particularly in non-CG context, is involved in TE regulation and dynamics under stress. Furthermore, we observed differential methylation for BPH adults and nymphs, emphasising the importance of screening juvenile life-stages in understanding adaptive-stress-responses in insects. Collectively, this study enhances our understanding of the role of transposons in influencing the evolutionary trajectory and survival strategies of BPH across generations.     

Host-finding behaviour in the nematode Pristionchus pacificus

Costs and benefits of foraging have been studied in predatory animals. In nematodes, ambushing or cruising behaviours represent adaptations that optimize foraging strategies for survival and host finding. A behaviour associated with host finding of ambushing nematode dauer juveniles is a sit-and-wait behaviour, otherwise known as nictation. Here, we test the function of nictation by relating occurrence of nictation in Pristionchus pacificus dauer juveniles to the ability to attach to laboratory host Galleria mellonella. We used populations of recently isolated and mutagenized laboratory strains. We found that nictation can be disrupted using a classical forward genetic approach and characterized two novel nictation-defective mutant strains. We identified two recently isolated strains from la Réunion island, one with a higher proportion of nictating individuals than the laboratory strain P. pacificus PS312. We found a positive correlation between nictation frequencies and host attachment in these strains. Taken together, our combination of genetic analyses with natural variation studies presents a new approach to the investigation of behavioural and ecological functionality. We show that nictation behaviour in P. pacificus nematodes serves as a host-finding behaviour. Our results suggest that nictation plays a role in the evolution of new life-history strategies, such as the evolution of parasitism.     

Behavioral evolution accompanying host shifts in cactophilic Drosophila larvae

For plant utilizing insects, the shift to a novel host is generally accompanied by a complex set of phenotypic adaptations. Many such adaptations arise in response to differences in plant chemistry, competitive environment, or abiotic conditions. One less well‐understood factor in the evolution of phytophagous insects is the selective environment provided by plant shape and volume. Does the physical structure of a new plant host favor certain phenotypes? Here, we use cactophilic Drosophila, which have colonized the necrotic tissues of cacti with dramatically different shapes and volumes, to examine this question. Specifically, we analyzed two behavioral traits in larvae, pupation height, and activity that we predicted might be related to the ability to utilize variably shaped hosts. We found that populations of D. mojavensis living on lengthy columnar or barrel cactus hosts have greater activity and pupate higher in a laboratory environment than populations living on small and flat prickly pear cactus cladodes. Crosses between the most phenotypically extreme populations suggest that the genetic architectures of these behaviors are distinct. A comparison of activity in additional cactophilic species that are specialized on small and large cactus hosts shows a consistent trend. Thus, we suggest that greater motility and an associated tendency to pupate higher in the laboratory are potential larval adaptations for life on a large plant where space is more abundant and resources may be more sparsely distributed.