Life-history Evolution Research Articles

Effects of development and parental care on Hamilton's force of selection.

The force of selection describes the sensitivity of population growth to changes in life history parameters, with a focus usually on the survival probabilities from one age class to the next. Importantly, according to Hamilton the force of selection generally decreases after the onset of reproduction, thereby providing a possible explanation for patterns of senescence. A second characteristic feature is that the force of selection remains constant up to the age of first re- production. This latter observation, however, rests on the assumption that offspring become independent from their parents right after birth. I show here in a minimal model that if offspring are fully reliant on their parents, either during early embryonal development or via parental care at later stages, and during this time prevent their parents from entering a new bout of repro- duction, the force of selection on offspring survival generally increases up until the age at which offspring become independent. This provides a possible explanation for the commonly observed pattern of decreasing mortality during early ontogeny. Further, genes acting during recurrent life stages are observed to experience a heightened force of selection compared to genes that act strictly age-specifically, demonstrating the need to develop a mechanistic understanding of gene activation patterns through which to consider life history evolution.

Evolution of mate harm resistance in females from Drosophila melanogaster populations selected for faster development and early reproduction.

Interlocus sexual conflict is predicted to result in sexually antagonistic coevolution between male competitive traits, which are also female-detrimental, and mate harm resistance (MHR) in females. Little is known about the connection between life-history evolution and sexually antagonistic coevolution. Here, we investigated the evolution of MHR in a set of experimentally evolved populations, where mate-harming ability has been shown to have substantially reduced in males as a correlated response to the selection for faster development and early reproduction. We measured mortality and fecundity of females of these populations and those of their matched controls, under different male exposure conditions. We observed that the evolved females were more susceptible to mate harm - suffering from significantly higher mortality under continuous exposure to control males within the twenty-day assay period. Though these evolved females are known to have shorter lifespan, substantially higher mortality was not observed under virgin and single-mating conditions. We used fecundity data to show that this higher mortality in the experimentally evolved females was not due to the cost of egg production, and hence can only be attributed to reduced MHR. Further analysis indicated that this decreased MHR is unlikely to be due purely to the smaller size of these females. Instead, it is more likely to be an indirect experimentally evolved response attributable to the changed breeding ecology, and/or male trait evolution. Our results underline the implications of changes in life history traits, including lifespan, to the evolution of MHR in females.

Developmental Pathways and Adjustment of Adult Women Who Experienced Early Pubertal Development: A Mixed-Method Approach

Early maturation among girls is a major stressful event that might affect their development and wellbeing during the adolescent years. However, the research literature is inconsistent as to whether the impact of early maturation among girls continues into their adult life. Taking a narrative approach, 45 adult women were interviewed and asked to describe their developmental life history following early maturation. Further, they reported on their wellbeing and body image. Analysis of the interviews yielded three developmental pathways: women for whom early maturation still impacts their daily life; women who were able to cope with the premature puberty and function well, but are still bothered by issues of body image; and women for whom early maturation served as an incentive for personal growth, who reported a high level of wellbeing, and comfort with their body. Findings underscore the importance of considering individual differences and different pathways of development among individuals.

Transcriptomic data support phylogenetic congruence and reveal genomic changes associated with the repeated evolution of annualism in aplocheiloid killifishes (Cyprinodontiformes)

Repeated evolution of novel life histories that are correlated with ecological variables offers opportunities to study convergence in genetic, developmental, and metabolic features. Nearly half of the 800 species of Aplocheiloid killifishes, a clade of teleost fishes with a circumtropical distribution, are “annual” or seasonal species that survive in ephemeral bodies of water that desiccate and are unfeasible for growth, reproduction, or survival for weeks to months every year. But the repeated evolution of adaptations that are key features of the annual life history among these fishes remains poorly known without a robust phylogenetic framework. We present a large-scale phylogenomic reconstruction of aplocheiloid killifishes evolution using newly sequenced transcriptomes obtained from a diversity of killifish lineages representing putative independent origins of annualism. Ancestral state estimation shows that developmental dormancy (diapause), a key trait of the killifish annual life cycle, may have originated up to seven times independently among African and South American lineages. To further explore the genetic basis of this unique trait, we measure changes in evolutionary rates among orthologous genes across the killifish tree of life by quantifying codon evolution using dN/dS ratios. We show that some genes have higher dN/dS ratios in lineages leading to species with annual life history. Many of them constitute key developmental genes or nuclear-encoded metabolic genes that control oxidative phosphorylation. Lastly, we compare these genes with higher ω to genes previously associated to developmental dormancy and metabolic shifts in killifishes and other vertebrates, and thereby identify molecular evolutionary signatures of repeated transitions to extreme environments.

Does childhood adversity make adolescents more morally disengaged? The effect of life history strategy and self-compassion

Childhood adversity may place adolescents at risk for moral disengagement. Drawing on evolutionary life history theory, this study aims to examine the underexplored relationship between childhood adversity and moral disengagement in Chinese adolescents as well as to explore the mediating role of life history strategy and the moderating role of self-compassion in the focal relationship. In Study 1, a total of 5089 adolescents were recruited and they finished a set of questionnaires concerning childhood adversity, life history strategy, self-compassion, and moral disengagement. A positive association was found between childhood adversity and moral disengagement via life history strategy, and this mediation effect was much weaker for adolescents who have high self-compassion. In Study 2, a total of 1890 adolescents initially participated in a three-wave longitudinal survey to validate the model obtained in Study 1. Childhood adversity increased adolescents' subsequent moral disengagement by accelerating their life history strategies, and self-compassion buffered the relatively long-lasting detrimental effects of childhood adversity. This work not only advances our understanding of the significant role of childhood adversity in causing moral disengagement among adolescents but also offers valuable insights into implementing appropriate preventions and interventions to reduce moral disengagement in adolescents and promote their positive development.

Bigger genomes provide environment-dependent growth benefits in grasses.

Increasing genome size (GS) has been associated with slower rates of DNA replication and greater cellular nitrogen (N) and phosphorus demands. Despite most plant species having small genomes, the existence of larger GS species suggests that such costs may be negligible or represent benefits under certain conditions. Focussing on the widespread and diverse grass family (Poaceae), we used data on species' climatic niches and growth rates under different environmental conditions to test for growth costs or benefits associated with GS. The influence of photosynthetic pathway, life history and evolutionary history on grass GS was also explored. We found that evolutionary history, photosynthetic pathway and life history all influence the distribution of grass species' GS. Genomes were smaller in annual and C4 species, the latter allowing for small cells necessary for C4 leaf anatomy. We found larger GS were associated with high N availability and, for perennial species, low growth-season temperature. Our findings reveal that GS is a globally important predictor of grass performance dependent on environmental conditions. The benefits for species with larger GS are likely due to associated larger cell sizes, allowing rapid biomass production where soil fertility meets N demands and/or when growth occurs via temperature-independent cell expansion.

Biotic and abiotic factors associated with genome size evolution in oaks.

The evolutionary processes that underlie variation in plant genome size have been much debated. Abiotic factors are thought to have played an important role, with negative and positive correlations between genome size and seasonal or stressful climatic conditions being reported in several systems. In turn, variation in genome size may influence plant traits which affect interactions with other organisms, such as herbivores. The mechanisms underlying evolutionary linkages between plant genome size and biotic and abiotic factors nonetheless remain poorly understod. To address this gap, we conducted phylogenetically controlled analyses testing for associations between genome size, climatic variables, plant traits (defenses and nutrients), and herbivory across 29 oak (Quercus) species. Genome size is significantly associated with both temperature and precipitation seasonality, whereby oak species growing in climates with lower and less variable temperatures but more variable rainfall had larger genomes. In addition, we found a negative association between genome size and leaf nutrient concentration (found to be the main predictor of herbivory), which in turn led to an indirect effect on herbivory. A follow-up test suggested that the association between genome size and leaf nutrients influencing herbivory was mediated by variation in plant growth, whereby species with larger genomes have slower growth rates, which in turn are correlated with lower nutrients. Collectively, these findings reveal novel associations between plant genome size and biotic and abiotic factors that may influence life history evolution and ecological dynamics in this widespread tree genus.

Cumulative and interannual effects of reproduction in eastern grey kangaroos.

Reproduction can reduce energy allocation to other life-history traits such as survival and growth. Resource constraints give rise to (co)variation in life-history traits and to heterogeneity in energy acquisition and allocation. At each reproductive opportunity, females face a choice between allocation to current reproduction or to maintenance. Many studies compare reproductive trade-offs between two consecutive years, but few account for the cumulative effects of reproduction over multiple years, a crucial factor in understanding life-history evolution in long-lived iteroparous species. We compared short- (interannual) and long-term (cumulative) reproductive trade-offs with a 14-year capture-mark-recapture study of eastern grey kangaroos, where females can have substantial skeletal growth for several years after maturation. We used a multivariate approach to compare how interannual and multi-annual cumulative reproduction affected growth (n = 378 measurements), mass change (n = 376 measurements) and subsequent reproduction (n = 388 measurements), and to quantify (co)variation between these traits among individuals (n = 107) and years (n = 14). Interannually, young females that reproduced experienced decreased skeletal growth compared to young females that did not reproduce. Reproductive females of all ages experienced reduced mass gain and weaning probability in the following year. The cumulative effects of multiple reproductions included decreased skeletal growth, mass gain and weaning probability in the following year. These effects increased with age and reproductive rate. We found positive trait correlations between mass change, leg growth and subsequent reproduction among individuals and years, though weaker at the cumulative than interannual level. Females experience dynamic interannual and cumulative trade-offs. Our analyses of cumulative costs of reproduction revealed long-term trade-offs as well as cumulative costs that were not apparent when estimating interannual costs. Trait correlations suggested heterogeneity in growth and reproduction among females. Years of increased growth were followed by years of increased reproduction, and years of poor growth were followed by years of poor reproduction. Our exploration of both interannual and cumulative costs of reproduction underscores the need to account for long-term reproductive histories to better understand reproductive trade-offs in long-lived iteroparous species.

Masting and Efficient Production of Seedlings: Balancing Costs of Variation Through Synchronised Fruiting.

The efficient conversion of tissues into reproductive success is a crucial aspect affecting the evolution of life histories. Masting, the interannually variable and synchronous seed production in perennial plants, is a strategy that can enhance reproductive efficiency by mitigating seed predation and pollen limitation. However, evaluating benefits is insufficient to establish whether efficiency has improved, as such assessments neglect the associated costs of masting, particularly during the critical seed-to-seedling stage. We conducted a parentage analysis of seedlings and adults in a population of 209 Sorbus aucuparia trees, monitored over 23 years, providing pioneering documentation of the effects of masting on the fitness of individual trees beyond the seed stage. Our results show high costs of interannual variation that can be mitigated by high synchrony and reveal the existence of phenotypes that appear to reap the benefits of masting while avoiding its costs through regular reproduction.

Lifetime trajectories of male mating effort under reproductive conflict in a cooperatively breeding mammal.

The costs of reproductive conflict can shape the evolution of life-histories in animal societies. These costs may change as individuals age and grow, and with within-group competition. Social costs of reproductive conflict have been invoked to explain why females might gain from delaying maturity or ceasing reproduction midway through life, but not in males. Here, we analyse more than 20 years of data to understand how individual male banded mongooses adjust their reproductive activity in response to the costs of reproductive conflict. In banded mongoose groups, multiple female breeders enter oestrus synchronously that are each guarded by a single male that aggressively wards-off rivals. The heaviest males in the group gained the greatest share of paternity. Those lighter males that are reproductively active paid disproportionate survival costs, and by engaging in reproductive activity early had lower lifetime reproductive success. Our results suggest that reproductive inactivity early in life is adaptive, as males recoup any lost fitness by first growing before engaging in less costly and more profitable reproductive activity later in life. These results suggest that resource holding potential of males and the intensity of reproductive conflict interact to shape lifetime schedules of reproductive behaviour.

Introduction to the Symposium: An Integrative Look at Whole-organism Trade-offs from the Female-centered Perspective of Biology.

Trade-offs during reproduction have long been a central focus within biology and much of the foundational work within life history evolution has focused on females, as the fitness of females is more easily quantified for use in theoretical models. However, in many regards, the field of organismal biology has deviated from this early focus on females, particularly as it relates to the nuances and dynamic nature of female reproduction. Regardless, at the organismal level, reproduction is thought to trade-off with other simultaneously occurring processes. Recent papers have sought to outline the issues with our current understanding of whole-organism trade-offs, though the field as a whole has not come to a consensus on what trade-offs mean to a reproducing female. To rectify this important gap in how trade-offs are discussed in organismal biology as well as confusion about what constitutes a trade-off, our overarching goal of this symposium was to discuss trade-offs from an integrative perspective that places female reproduction at the center. By answering what trade-offs are and what they mean to reproducing females, what has been neglected in the context of whole-organism physiology, and how maternal effects fit within this framework, our group of speakers and their associated papers will crystalize nuances of measuring and determining presence (if any) of trade-offs in reproducing females in a range of taxa and subfields.

Evolutionary transitions of decapod crustaceans to non-marine, polar, and deep-sea environments: developmental, physiological and biochemical adaptations

Abstract In this brief, non-exhaustive essay, we review major adaptive changes in reproductive and developmental traits of decapod crustaceans, which have passed through evolutionary transitions from ancestral life in coastal marine environments to brackish, limnic, polar, or deep-sea habitats. Two major approaches can be recognised in studies of life-history evolution, focussing on: (1) developmental changes in adaptive physiological or biochemical traits of successive ontogenetic stages, comparing, for instance, osmoregulatory capabilities in larvae, juveniles, and adults (“ontogeny of adaptations” perspective); (2) adaptive changes in the modes of reproduction and development, e.g., enhanced maternal energy investment in egg production, abbreviated, non-feeding larval development (“adaptations in ontogeny”). Using both scientific approaches, Christoph D. Schubart has significantly contributed to our understanding of evolutionary transitions in crustaceans. In our essay, we pay particular attention to the significance of nutritional selection factors in relation to presumably adaptive developmental, physiological, and biochemical traits in different life-history stages. In this context, we highlight the key roles of lipids and carotenoid pigments, in particular of essential polyunsaturated fatty acids (PUFAs) and astaxanthin. While PUFAs and other lipid compounds have received wide scientific attention, we propose that future studies should further analyse also the potential role of astaxanthin and other essential carotenoids.

Complex ontogeny of sexual size dimorphism in a female-larger gecko: Implications of determinate growth for lizard body size and life-history evolution.

Ectothermic vertebrates such as reptiles were assumed to be indeterminate growers, which means that there is no terminal point in time or size for growth in their lifetime. In recent years, evidence for the determinate nature of growth in lizards has accumulated, necessitating a re-examination of models of their ontogeny and evolution of sexual size dimorphism (SSD). In the female-larger gecko Paroedura vazimba, we monitored post-embryonic growth over a period of 15 months. After hatching, females grew faster than males but also reached their final body size, that is, closed growth of their vertebrae, earlier than males. The closure of bone growth in females correlates with the onset of reproductive maturation. We compared this pattern with the previously minutely studied, male-larger species Paroedura picta, where we documented determinate growth as well. We propose a model to explain the evolutionary switches in the direction of SSD in lizards based on bipotential effects of ovarian hormones on growth. In this model, male growth is assumed to require no male-specific growth modifier, such as sex-limited hormonal regulators, while growth is feminized by ovarian hormones in females. Low levels of ovarian hormones can promote bone growth, but high levels associated with maturation of the reproductive organs promote senescence of bone growth plates and thus cessation of bone growth. We suggest that models on growth, life-history and evolution of body size in many lizards should acknowledge their determinate nature of growth.

Genome and life-history evolution link bird diversification to the end-Cretaceous mass extinction.

Complex patterns of genome evolution associated with the end-Cretaceous [Cretaceous-Paleogene (K-Pg)] mass extinction limit our understanding of the early evolutionary history of modern birds. Here, we analyzed patterns of avian molecular evolution and identified distinct macroevolutionary regimes across exons, introns, untranslated regions, and mitochondrial genomes. Bird clades originating near the K-Pg boundary exhibited numerous shifts in the mode of molecular evolution, suggesting a burst of genomic heterogeneity at this point in Earth's history. These inferred shifts in substitution patterns were closely related to evolutionary shifts in developmental mode, adult body mass, and patterns of metabolic scaling. Our results suggest that the end-Cretaceous mass extinction triggered integrated patterns of evolution across avian genomes, physiology, and life history near the dawn of the modern bird radiation.

Income and Sex Moderate the Association Between Population Density and Reproduction: A Multilevel Analysis of Life History Strategies Across 23 Nations.

While previous studies guided by evolutionary life history theory have revealed several important socioecological moderators of the influence of population density (PD) on reproduction, absent is an understanding of how individual-level factors such as personal resources and sex differences might interact and play a role. Using data from a large sample of clients (N = 4,432,440) of an online dating company spanning 317 states nested within 23 countries, we contributed a robust multilevel analysis of life history effects by assessing the interaction between state-level PD and individual-level income on offspring quantity, and we further qualified this analysis by sex. Consistent with previous research, PD was negatively correlated with having children. Consistent with our novel hypotheses, this negative relationship was moderated by income such that the link between PD and low fertility became weaker with increasing levels of income and these patterns were stronger for men than for women. These results held despite controlling for a variety of country-level, state-level, and individual-level confounds. Findings are discussed together with theoretical and practical implications for the management of fertility based on evolutionary life history perspectives.

Primary Cell Culture as a Model System for Evolutionary Molecular Physiology.

Primary cell culture is a powerful model system to address fundamental questions about organismal physiology at the cellular level, especially for species that are difficult, or impossible, to study under natural or semi-natural conditions. Due to their ease of use, primary fibroblast cultures are the dominant model system, but studies using both somatic and germ cells are also common. Using these models, genome evolution and phylogenetic relationships, the molecular and biochemical basis of differential longevities among species, and the physiological consequences of life history evolution have been studied in depth. With the advent of new technologies such as gene editing and the generation of induced pluripotent stem cells (iPSC), the field of molecular evolutionary physiology will continue to expand using both descriptive and experimental approaches.

Playing it safe? An evolutionary life history theory perspective on Canadian adolescent play during the COVID-19 pandemic

ABSTRACT Playing during adolescence is hypothesized to prepare young people to respond to unexpected future challenges. But, when extrinsic environmental risks are high, adolescents are expected to prioritize immediate-payoff behaviours over playing. It is unclear, though, how an ecological shock like a spike in community spread of a potentially deadly virus might affect adolescent play. Using data from a socio-demographically-diverse sample of 460 Canadian adolescents surveyed across varying levels of threat/restrictions during the COVID-19 pandemic, of whom 39 also engaged in focus groups, we explored variations in time allocations to play. We regressed indicators of respondents' time spent on play on whether they responded during a pandemic wave peak, and on socio-ecological-demographic parameters. Health indicators were then regressed on the play. Focus group quotes and perspectives contextualized the quantitative findings. There was no clear evidence of changes in overall time allocations to play during increased viral threat/restrictions, but modes of play were atypical for adolescents, regardless of when they responded. Adolescents living under more stressful socio-ecological conditions engaged in less play. The play was positively associated with health indicators. Pandemic spikes did not reduce the time Canadian adolescents spent playing, but likely affected how they played, which has implications for their current and future well-being.

Integrative analyses on the ciliates Colpoda illuminate the life history evolution of soil microorganisms.

Microorganisms play a central role in sustaining soil ecosystems and agriculture, and these functions are usually associated with their complex life history. Yet, the regulation and evolution of life history have remained enigmatic and poorly understood, especially in protozoa, the third most abundant group of organisms in the soil. Here, we explore the life history of a cosmopolitan species-Colpoda steinii. Our analysis has yielded a high-quality macronuclear genome for C. steinii, with size of 155 Mbp and 37,123 protein-coding genes, as well as mean intron length of ~93 bp, longer than most other studied ciliates. Notably, we identify two possible whole-genome duplication events in C. steinii, which may account for its genome being about twice the size of C. inflata's, another co-existing species. We further resolve the gene expression profiles in diverse life stages of C. steinii, which are also corroborated in C. inflata. During the resting cyst stage, genes associated with cell death and vacuole formation are upregulated, and translation-related genes are downregulated. While the translation-related genes are upregulated during the excystment of resting cysts. Reproductive cysts exhibit a significant reduction in cell adhesion. We also demonstrate that most genes expressed in specific life stages are under strong purifying selection. This study offers a deeper understanding of the life history evolution that underpins the extraordinary success and ecological functions of microorganisms in soil ecosystems.IMPORTANCEColpoda species, as a prominent group among the most widely distributed and abundant soil microorganisms, play a crucial role in sustaining soil ecosystems and promoting plant growth. This investigation reveals their exceptional macronuclear genomic features, including significantly large genome size, long introns, and numerous gene duplications. The gene expression profiles and the specific biological functions associated with the transitions between various life stages are also elucidated. The vast majority of genes linked to life stage transitions are subject to strong purifying selection, as inferred from multiple natural strains newly isolated and deeply sequenced. This substantiates the enduring and conservative nature of Colpoda's life history, which has persisted throughout the extensive evolutionary history of these highly successful protozoa in soil. These findings shed light on the evolutionary dynamics of microbial eukaryotes in the ever-fluctuating soil environments. This integrative research represents a significant advancement in understanding the life histories of these understudied single-celled eukaryotes.

Diversity of major histocompatibility complex of II B gene and mate choice in a monogamous and long-lived seabird, the Little Auk (Alle alle).

The major histocompatibility complex (MHC) plays a key role in the adaptive immune system of vertebrates, and is known to influence mate choice in many species. In birds, the MHC has been extensively examined but mainly in galliforms and passerines while other taxa that represent specific ecological and evolutionary life-histories, like seabirds, are underexamined. Here, we characterized diversity of MHC Class II B exon 2 in a colonial pelagic seabird, the Little Auk (or Dovekie Alle alle). We further examined whether MHC variation could be maintained through balancing selection and disassortative mating. We found high polymorphism at the genotyped MHC fragment, characterizing 99 distinct alleles across 140 individuals from three populations. The alleles frequencies exhibited a similar skewed distribution in both sexes, with the four most commonly occurring alleles representing approximately 35% of allelic variation. The results of a Bayesian site-by-site selection analysis suggest evidence of balancing selection and no direct evidence for MHC-dependent disassortative mating preferences in the Little Auk. The latter result might be attributed to the high overall polymorphism of the examined fragment, which itself may be maintained by the large population size of the species.

A somatic genetic clock for clonal species

Age and longevity are key parameters for demography and life-history evolution of organisms. In clonal species, a widespread life history among animals, plants, macroalgae and fungi, the sexually produced offspring (genet) grows indeterminately by producing iterative modules, or ramets, and so obscure their age. Here we present a novel molecular clock based on the accumulation of fixed somatic genetic variation that segregates among ramets. Using a stochastic model, we demonstrate that the accumulation of fixed somatic genetic variation will approach linearity after a lag phase, and is determined by the mitotic mutation rate, without direct dependence on asexual generation time. The lag phase decreased with lower stem cell population size, number of founder cells for the formation of new modules, and the ratio of symmetric versus asymmetric cell divisions. We calibrated the somatic genetic clock on cultivated eelgrass Zostera marina genets (4 and 17 years respectively). In a global data set of 20 eelgrass populations, genet ages were up to 1,403 years. The somatic genetic clock is applicable to any multicellular clonal species where the number of founder cells is small, opening novel research avenues to study longevity and, hence, demography and population dynamics of clonal species.