DO VARIATIONS IN SUBSTITUTION RATES AND MALE MUTATION BIAS CORRELATE WITH LIFE‐HISTORY TRAITS? A STUDY OF 32 MAMMALIAN GENOMES

Life-history traits vary substantially across species, and have been demonstrated to affect substitution rates. We compute genome-wide, branch-specific estimates of male mutation bias (the ratio of male-to-female mutation rates) across 32 mammalian genomes and study how these vary with life-history traits (generation time, metabolic rate, and sperm competition). We also investigate the influence of life-history traits on substitution rates at unconstrained sites across a wide phylogenetic range. We observe that increased generation time is the strongest predictor of variation in both substitution rates (for which it is a negative predictor) and male mutation bias (for which it is a positive predictor). Although less significant, we also observe that estimates of metabolic rate, reflecting replication-independent DNA damage and repair mechanisms, correlate negatively with autosomal substitution rates, and positively with male mutation bias. Finally, in contrast to expectations, we find no significant correlation between sperm competition and either autosomal substitution rates or male mutation bias. Our results support the important but frequently opposite effects of some, but not all, life-history traits on substitution rates.     

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.     

Multi-objective optimization shapes ecological variation

Ecological systems contain a huge amount of quantitative variation between and within species and locations, which makes it difficult to obtain unambiguous verification of theoretical predictions. Ordinary experiments consider just a few explanatory factors and are prone to providing oversimplified answers because they ignore the complexity of the factors that underlie variation. We used multi-objective optimization (MO) for a mechanistic analysis of the potential ecological and evolutionary causes and consequences of variation in the life-history traits of a species of moth. Optimal life-history solutions were sought for environmental conditions where different life stages of the moth were subject to predation and other known fitness-reducing factors in a manner that was dependent on the duration of these life stages and on variable mortality rates. We found that multi-objective optimal solutions to these conditions that the moths regularly experience explained most of the life-history variation within this species. Our results demonstrate that variation can have a causal interpretation even for organisms under steady conditions. The results suggest that weather and species interactions can act as underlying causes of variation, and MO acts as a corresponding adaptive mechanism that maintains variation in the traits of organisms.     

Life-history correlates of maximum population growth rates in marine fishes

Theory predicts that populations of animals with late maturity, low fecundity, large body size and low body growth rates will have low potential rates of population increase at low abundance. If this is true, then these traits may be used to predict the intrinsic rate of increase for species or populations, as well as extinction risks. We used life-history and population data for 63 stocks of commercially exploited fish species from the northeast Atlantic to test relationships between life-history parameters and the rate of population increase at low abundance. We used cross-taxonomic analyses among stocks and among species, and analyses that accounted for phylogenetic relationships. These analyses confirmed that large-bodied, slow-growing stocks and species had significantly lower rates of recruitment and adult production per spawning adult at low abundance. Furthermore, high ages at maturity were significantly correlated with low maximum recruit production. Contrary to expectation, fecundity was significantly negatively related to recruit production, due to its positive relationship with maximum body size. Our results support theoretical predictions, and suggest that a simply measured life-history parameter can provide a useful tool for predicting rates of recovery from low population abundance.     

Are animal personality traits linked to life-history productivity?

Animal personality traits such as boldness, activity and aggressiveness have been described for many animal species. However, why some individuals are consistently bolder or more active than others, for example, is currently obscure. Given that life-history tradeoffs are common and known to promote inter-individual differences in behavior, we suggest that consistent individual differences in animal personality traits can be favored when those traits contribute to consistent individual differences in productivity (growth and/or fecundity). A survey of empirical studies indicates that boldness, activity and/or aggressiveness are positively related to food intake rates, productivity and other life-history traits in a wide range of taxa. Our conceptual framework sets the stage for a closer look at relationships between personality traits and life-history traits in animals.     

Joint reconstruction of divergence times and life-history evolution in placental mammals using a phylogenetic covariance model

Violation of the molecular clock has been amply documented, and is now routinely taken into account by molecular dating methods. Comparative analyses have revealed a systematic component in rate variation, relating it to the evolution of life-history traits, such as body size or generation time. Life-history evolution can be reconstructed using Brownian models. However, the resulting estimates are typically uncertain, and potentially sensitive to the underlying assumptions. As a way of obtaining more accurate ancestral trait and divergence time reconstructions, correlations between life-history traits and substitution rates could be used as an additional source of information. In this direction, a Bayesian framework for jointly reconstructing rates, traits, and dates was previously introduced. Here, we apply this model to a 17 protein-coding gene alignment for 73 placental taxa. Our analysis indicates that the coupling between molecules and life history can lead to a reevaluation of ancestral life-history profiles, in particular for groups displaying convergent evolution in body size. However, reconstructions are sensitive to fossil calibrations and to the Brownian assumption. Altogether, our analysis suggests that further integrating inference of rates and traits might be particularly useful for neontological macroevolutionary comparative studies.     

Rates of molecular evolution in bacteria are relatively constant despite spore dormancy

Rates of molecular evolution are known to vary considerably among lineages, partially due to differences in life-history traits such as generation time. The generation-time effect has been well documented in some eukaryotes, but its prevalence in prokaryotes is unknown. "Because many species of Firmicute bacteria spend long periods of time as metabolically dormant spores, which could result in fewer DNA substitutions per unit time, they present an excellent system for testing predictions of the molecular clock hypothesis." To test whether spore-forming bacteria evolve more slowly than their non-spore-forming relatives, I used phylogenetic methods to determine if there were differences in rates of amino acid substitution between spore-forming and non-spore-forming lineages of Firmicute bacteria. Although rates of evolution do vary among lineages, I find no evidence for an effect of spore-formation on evolutionary rate and, furthermore, evolutionary rates are similar to those calculated for enteric bacteria. These results support the notion that variation in generation time does not affect evolutionary rates in bacterial lineages.     

Meta-analysis suggests choosy females get sexy sons more than "good genes"

Female preferences for specific male phenotypes have been documented across a wide range of animal taxa, including numerous species where males contribute only gametes to offspring production. Yet, selective pressures maintaining such preferences are among the major unknowns of evolutionary biology. Theoretical studies suggest that preferences can evolve if they confer genetic benefits in terms of increased attractiveness of sons ("Fisherian" models) or overall fitness of offspring ("good genes" models). These two types of models predict, respectively, that male attractiveness is heritable and genetically correlated with fitness. In this meta-analysis, we draw general conclusions from over two decades worth of empirical studies testing these predictions (90 studies on 55 species in total). We found evidence for heritability of male attractiveness. However, attractiveness showed no association with traits directly associated with fitness (life-history traits). Interestingly, it did show a positive correlation with physiological traits, which include immunocompetence and condition. In conclusion, our results support "Fisherian" models of preference evolution, while providing equivocal evidence for "good genes." We pinpoint research directions that should stimulate progress in our understanding of the evolution of female choice.     

DOES TOTAL REPRODUCTIVE EFFORT EVOLVE INDEPENDENTLY OF OFFSPRING SIZE?

In all species, patterns of reproductive allocation have important fitness consequences and therefore important implications for life-history evolution. Nearly universally, theory in this field has modeled as independent the evolution of total allocation to offspring and the subsequent division of this allocation into many small versus few large offspring. Yet, some theory and a very small amount of experimental evidence suggest that these life-history traits may be evolutionarily linked. Using comparative analyses of copepod life histories, we illustrate that rather than being evolutionarily independent these traits can be linked, in this case, across a very large clade of invertebrates. Our results indicate that a more complete understanding of the evolution of these traits will require greater consideration of simultaneous allocation decisions, rather than sequential ones, and other genetic and selective mechanisms.     

Host responses in life-history traits and tolerance to virus infection in Arabidopsis thaliana

Knowing how hosts respond to parasite infection is paramount in understanding the effects of parasites on host populations and hence host-parasite co-evolution. Modification of life-history traits in response to parasitism has received less attention than other defence strategies. Life-history theory predicts that parasitised hosts will increase reproductive effort and accelerate reproduction. However, empirical analyses of these predictions are few and mostly limited to animal-parasite systems. We have analysed life-history trait responses in 18 accessions of Arabidopsis thaliana infected at two different developmental stages with three strains of Cucumber mosaic virus (CMV). Accessions were divided into two groups according to allometric relationships; these groups differed also in their tolerance to CMV infection. Life-history trait modification upon virus infection depended on the host genotype and the stage at infection. While all accessions delayed flowering, only the more tolerant allometric group modified resource allocation to increase the production of reproductive structures and progeny, and reduced the length of reproductive period. Our results are in agreement with modifications of life-history traits reported for parasitised animals and with predictions from life-history theory. Thus, we provide empirical support for the general validity of theoretical predictions. In addition, this experimental approach allowed us to quantitatively estimate the genetic determinism of life-history trait plasticity and to evaluate the role of life-history trait modification in defence against parasites, two largely unexplored issues.     

The erratic mitochondrial clock: variations of mutation rate, not population size, affect mtDNA diversity across birds and mammals

Background  

During the last ten years, major advances have been made in characterizing and understanding the evolution of mitochondrial DNA, the most popular marker of molecular biodiversity. Several important results were recently reported using mammals as model organisms, including (i) the absence of relationship between mitochondrial DNA diversity and life-history or ecological variables, (ii) the absence of prominent adaptive selection, contrary to what was found in invertebrates, and (iii) the unexpectedly large variation in neutral substitution rate among lineages, revealing a possible link with species maximal longevity. We propose to challenge these results thanks to the bird/mammal comparison. Direct estimates of population size are available in birds, and this group presents striking life-history trait differences with mammals (higher mass-specific metabolic rate and longevity). These properties make birds the ideal model to directly test for population size effects, and to discriminate between competing hypotheses about the causes of substitution rate variation.     

Ecological Equivalence: A Realistic Assumption for Niche Theory as a Testable Alternative to Neutral Theory

Background

Hubbell''s 2001 neutral theory unifies biodiversity and biogeography by modelling steady-state distributions of species richness and abundances across spatio-temporal scales. Accurate predictions have issued from its core premise that all species have identical vital rates. Yet no ecologist believes that species are identical in reality. Here I explain this paradox in terms of the ecological equivalence that species must achieve at their coexistence equilibrium, defined by zero net fitness for all regardless of intrinsic differences between them. I show that the distinction of realised from intrinsic vital rates is crucial to evaluating community resilience.

Principal Findings

An analysis of competitive interactions reveals how zero-sum patterns of abundance emerge for species with contrasting life-history traits as for identical species. I develop a stochastic model to simulate community assembly from a random drift of invasions sustaining the dynamics of recruitment following deaths and extinctions. Species are allocated identical intrinsic vital rates for neutral dynamics, or random intrinsic vital rates and competitive abilities for niche dynamics either on a continuous scale or between dominant-fugitive extremes. Resulting communities have steady-state distributions of the same type for more or less extremely differentiated species as for identical species. All produce negatively skewed log-normal distributions of species abundance, zero-sum relationships of total abundance to area, and Arrhenius relationships of species to area. Intrinsically identical species nevertheless support fewer total individuals, because their densities impact as strongly on each other as on themselves. Truly neutral communities have measurably lower abundance/area and higher species/abundance ratios.

Conclusions

Neutral scenarios can be parameterized as null hypotheses for testing competitive release, which is a sure signal of niche dynamics. Ignoring the true strength of interactions between and within species risks a substantial misrepresentation of community resilience to habitat loss.     

Co-Gradient Variation in Growth Rate and Development Time of a Broadly Distributed Butterfly

Widespread species often show geographic variation in thermally-sensitive traits, providing insight into how species respond to shifts in temperature through time. Such patterns may arise from phenotypic plasticity, genetic adaptation, or their interaction. In some cases, the effects of genotype and temperature may act together to reduce, or to exacerbate, phenotypic variation in fitness-related traits across varying thermal environments. We find evidence for such interactions in life-history traits of Heteronympha merope, a butterfly distributed across a broad latitudinal gradient in south-eastern Australia. We show that body size in this butterfly is negatively related to developmental temperature in the laboratory, in accordance with the temperature-size rule, but not in the field, despite very strong temperature gradients. A common garden experiment on larval thermal responses, spanning the environmental extremes of H. merope''s distribution, revealed that butterflies from low latitude (warmer climate) populations have relatively fast intrinsic growth and development rates compared to those from cooler climates. These synergistic effects of genotype and temperature across the landscape (co-gradient variation) are likely to accentuate phenotypic variation in these traits, and this interaction must be accounted for when predicting how H. merope will respond to temperature change through time. These results highlight the importance of understanding how variation in life-history traits may arise in response to environmental change. Without this knowledge, we may fail to detect whether organisms are tracking environmental change, and if they are, whether it is by plasticity, adaptation or both.     

Individual covariation in life-history traits: seeing the trees despite the forest

We investigated the influence of age on survival and breeding rates in a long-lived species Rissa tridactyla using models with individual random effects permitting variation and covariation in fitness components among individuals. Differences in survival or breeding probabilities among individuals are substantial, and there was positive covariation between survival and breeding probability; birds that were more likely to survive were also more likely to breed, given that they survived. The pattern of age-related variation in these rates detected at the individual level differed from that observed at the population level. Our results provided confirmation of what has been suggested by other investigators: within-cohort phenotypic selection can mask senescence. Although this phenomenon has been extensively studied in humans and captive animals, conclusive evidence of the discrepancy between population-level and individual-level patterns of age-related variation in life-history traits is extremely rare in wild animal populations. Evolutionary studies of the influence of age on life-history traits should use approaches differentiating population level from the genuine influence of age: only the latter is relevant to theories of life-history evolution. The development of models permitting access to individual variation in fitness is a promising advance for the study of senescence and evolutionary processes.     

Seasonal plasticity in life history traits: growth and development in Polygonia c-album (Lepidoptera: Nymphalidae)

The potentially multivoltine comma butterfly, Polygonia c-album L., hibernates in the adult stage. The adult seasonal morph is demonstrated to be a good indicator of whether an individual has entered reproductive diapause or is developing directly to sexual maturation. This fact, and the assumption that a short development time is not equally important to all categories of individuals, was used to test predictions on variation in life-history traits among categories (morphs and sexes) and environments (temperature and photoperiod) at the level of individuals and to some extent families and populations (the univoltine Stockholm population and the partially bivoltine Oxford population). Individuals developing to adults in a short time were expected to be smaller and lighter as a result of a basic trade-off between the two traits. Development times varied in accordance with predictions, but in most cases this was due to plastic growth and development in both the larval and pupal stages rather than through variation in size or weight, i.e. size was a highly canalized trait. This suggests a relationship between plasticity and canalization and a strong potential for plasticity to shield life-history traits from selection. Individuals regulated development times also within developmental pathways, in response to photoperiods indicating the progression of the season. These and other results suggest that development times are not normally minimized in temperate butterflies unless this is enforced by direct development and protandry. There is thus scope for a high degree of adaptive plasticity in growth- and developmental rates which may devalue the basic trade-offs assumed by life-history theory and account for inconsistencies with its predictions.     

A perfect storm: the combined effects on population fluctuations of autocorrelated environmental noise, age structure, and density dependence

While it is widely appreciated that climate can affect the population dynamics of various species, a mechanistic understanding of how climate interacts with life-history traits to influence population fluctuations requires development. Here we build a general density-dependent age-structured model that accounts for differential responses in life-history traits to increasing population density. We show that as the temporal frequency of favorable environmental conditions increases, population fluctuations also increase provided that unfavorable environmental conditions still occur. As good years accumulate and the number of individuals in a population increases, successive life-history traits become vulnerable to density dependence once a return to unfavorable conditions prevails. The stronger this ratcheting of density dependence in life-history traits by autocorrelated climatic conditions, the larger the population fluctuations become. Highly fecund species, and those in which density dependence occurs in juvenile and adult vital rates at similar densities, are most sensitive to increases in the frequency of favorable conditions. Understanding the influence of global warming on temporal correlation in regional environmental conditions will be important in identifying those species liable to exhibit increased population fluctuations that could lead to their extinction.     

Dispersal as a source of variation in age-specific reproductive strategies in a wild population of lizards

Dispersal syndromes describe the patterns of covariation of morphological, behavioural, and life-history traits associated with dispersal. Studying dispersal syndromes is critical to understanding the demographic and genetic consequences of movements. Among studies describing the association of life-history traits with dispersal, there is anecdotal evidence suggesting that dispersal syndromes can vary with age. Recent theory also suggests that dispersive and philopatric individuals might have different age-specific reproductive efforts. In a wild population of the common lizard (Zootoca vivipara), we investigated whether dispersive and philopatric individuals have different age-specific reproductive effort, survival, offspring body condition, and offspring sex ratio. Consistent with theoretical predictions, we found that young dispersive females have a higher reproductive effort than young philopatric females. Our results also suggest that the early high investment in reproduction of dispersive females trades-off with an earlier onset of senescence than in philopatric females. We further found that young dispersive females produce smaller offspring in lower body condition than do young philopatric females. Overall, our results provide empirical evidence that dispersive and philopatric individuals have different age-specific life-history traits.     

Monthly survival of African Sylvia warblers in a seasonally arid tropical environment

Latitudinal gradients of life-history traits in animals are thought to be shaped by environmental variables. For example, it has been suggested that the increase in avian clutch size from the tropics towards the northern temperate regions is caused by a reduced survival of adult birds in the north due to increasing environmental seasonality. However, the tropical savannahs of East Africa show pronounced seasonality in resources caused by distinct rainy and dry seasons. This raises the question of whether survival and other life-history traits of birds living in these tropical savannahs are influenced by this seasonality, making them more similar to northern temperate species. We used 2-year monthly resighting data, a multistate modelling approach and the program MARK to test whether survival, transition probabilities between breeding states and other life-history traits of two resident Kenyan Sylvia species (Aves: Passeriformes: Sylviidae) are shaped by seasonality of rainfall in their environment. Contradicting our hypotheses, the two species showed only very slight influence of seasonality of rainfall on their survival. Survival in the dry months was hardly lower than in the rainy months. The species in the more seasonal environment ( S. boehmi , annual survival 71%) survived as well as the one in the more constant environment ( S. lugens , 56%). The observed survival rates correspond well to other life-history traits of the two species and are of similar magnitude to survival rates of other tropical passerines. This implies that either seasonality is not the driving force behind the life-history traits of the two species or the birds do not experience their environment as seasonal, as might be suggested by fluctuations in rainfall.     

Ecological and phylogenetic determinants of life-history patterns among ten loricariid species

We analysed the influence of ecological factors, phylogenetic history and trade-offs between traits on the life-history variation among 10 loricariid species of the middle Paraná River. We measured eight life-history variables and classified the life-history strategies following the equilibrium–periodic–opportunistic (EPO) model. Principal-component analysis of life-history traits segregated species along a gradient from small opportunistic (low fecundity, low parental investment) to large equilibrium (low-medium fecundity, high parental investment) species. A clear periodic strategist was absent in the analysed assemblage. Variation partitioning by canonical phylogenetic ordination analysis showed both a component of variation uniquely explained by phylogenetic history (PH; 32.2%) and a component shared between PH and ecological factors (EF; 37%). The EPO model is a useful tool for predicting correlations among life-history traits and understanding potential demographic responses of species to environmental variation. Life-history patterns observed throughout Loricariidae suggests that this family has diversified across all three endpoint strategies of the EPO model. Our study indicates that evolutionary lineage affiliation at the level of subfamily can be a strong predictor of the life-history strategy used by each species.     

The determinants of the molecular substitution process in turtles

Neutral rates of molecular evolution vary across species, and this variation has been shown to be related to biological traits. One of the first patterns to be observed in vertebrates has been an inverse relationship between body mass (BM) and substitution rates. The effects of three major life‐history traits (LHT) that covary with BM – metabolic rate, generation time and longevity (LON) – have been invoked to explain this relationship. However, most of the theoretical and empirical evidence supporting this relationship comes from endothermic vertebrates, that is, mammals and birds, in which the environmental conditions, especially temperature, do not have a direct impact on cellular and molecular biology. We analysed the variations in mitochondrial and nuclear rates of synonymous substitution across 224 turtle species and examined their correlation with two LHT (LON and BM) and two environmental variables [latitude (LAT) and habitat]. Our analyses indicate that in turtles, neutral rates of molecular evolution are hardly correlated with LON or BM. Rather, both the mitochondrial and nuclear substitution rates are significantly correlated with LAT – faster evolution in the tropics – and especially so for aquatic species. These results question the generality of the relationships reported in mammals and birds and suggest that environmental factors might be the strongest determinants of the mutation rate in ectotherms.