Individual life histories: neither slow nor fast, just diverse.

The slow-fast continuum is a commonly used framework to describe variation in life-history strategies across species. Individual life histories have also been assumed to follow a similar pattern, especially in the pace-of-life syndrome literature. However, whether a slow-fast continuum commonly explains life-history variation among individuals within a population remains unclear. Here, we formally tested for the presence of a slow-fast continuum of life histories both within populations and across species using detailed long-term individual-based demographic data for 17 bird and mammal species with markedly different life histories. We estimated adult lifespan, age at first reproduction, annual breeding frequency, and annual fecundity, and identified the main axes of life-history variation using principal component analyses. Across species, we retrieved the slow-fast continuum as the main axis of life-history variation. However, within populations, the patterns of individual life-history variation did not align with a slow-fast continuum in any species. Thus, a continuum ranking individuals from slow to fast living is unlikely to shape individual differences in life histories within populations. Rather, individual life-history variation is likely idiosyncratic across species, potentially because of processes such as stochasticity, density dependence, and individual differences in resource acquisition that affect species differently and generate non-generalizable patterns across species.

Inferring Transmission Histories of Rare Alleles in Population-Scale Genealogies.

Learning the transmission history of alleles through a family or population plays an important role in evolutionary, demographic, and medical genetic studies. Most classical models of population genetics have attempted to do so under the assumption that the genealogy of a population is unavailable and that its idiosyncrasies can be described by a small number of parameters describing population size and mate choice dynamics. Large genetic samples have increased sensitivity to such modeling assumptions, and large-scale genealogical datasets become a useful tool to investigate realistic genealogies. However, analyses in such large datasets are often intractable using conventional methods. We present an efficient method to infer transmission paths of rare alleles through population-scale genealogies. Based on backward-time Monte Carlo simulations of genetic inheritance, we use an importance sampling scheme to dramatically speed up convergence. The approach can take advantage of available genotypes of subsets of individuals in the genealogy including haplotype structure as well as information about the mode of inheritance and general prevalence of a mutation or disease in the population. Using a high-quality genealogical dataset of more than three million married individuals in the Quebec founder population, we apply the method to reconstruct the transmission history of chronic atrial and intestinal dysrhythmia (CAID), a rare recessive disease. We identify the most likely early carriers of the mutation and geographically map the expected carrier rate in the present-day French-Canadian population of Quebec.

Historical human remains identification through maternal and paternal genetic signatures in a founder population with extensive genealogical record.

OBJECTIVES: We describe a method to identify human remains excavated from unmarked graves in historical Québec cemeteries by combining parental-lineage genetic markers with the whole-population genealogy of Québec contained in the BALSAC database. MATERIALS AND METHODS: The remains of six men were exhumed from four historical cemeteries in the province of Québec, Canada. DNA was extracted from the remains and genotyped to reveal their mitochondrial and Y-chromosome haplotypes, which were compared to a collection of haplotypes of genealogically-anchored modern volunteers. Maternal and paternal genealogies were searched in the BALSAC genealogical record for parental couples matching the mitochondrial and the Y-chromosome haplotypic signatures, to identify candidate sons from whom the remains could have originated. RESULTS: Analysis of the matching genealogies identified the parents of one man inhumed in the cemetery of the investigated parish during its operating time. The candidate individual died in 1833 at the age of 58, a plausible age at death in light of osteological analysis of the remains. DISCUSSION: This study demonstrates the promising potential of coupling genetic information from living individuals to genealogical data in BALSAC to identify historical human remains. If genetic coverage is increased, the genealogical information in BALSAC could enable the identification of 87% of the men (n = 178,435) married in Québec before 1850, with high discriminatory power in most cases since >75% of the parental couples have unique biparental signatures in most regions. Genotyping and identifying Québec's historical human remains are a key to reconstructing the genomes of the founders of Québec and reinhuming archeological remains with a marked grave.

Into the wild-WAMBAM goes to Canada.

The sixth Wild Animal Models Bi-Annual Meeting was held in July 2017 in Québec, with 42 participants. This report documents the evolution of questions asked and approaches used in evolutionary quantitative genetic studies of wild populations in recent decades, and how these questions and approaches were represented at the recent meeting. We explore how ideas from previous meetings in this series have developed to their present states, and consider how the format of the meetings may be particularly useful at fostering the rapid development and proliferation of ideas and approaches.

Population genetic data of the AmpFℓSTR® Identifiler® Plus and PowerPlex® 16 HS STR loci in four Canadian populations.

Allele frequencies and forensically relevant population statistics were estimated for the short tandem repeat (STR) loci of the AmpFℓSTR® Identifiler® Plus and PowerPlex® 16 HS amplification kits, including D2S1338, D19S433, Penta D, and Penta E, for three First Nations Aboriginal populations and for Caucasians in Canada. The cumulative power of discrimination was ≥ 0.999999999999984 and the cumulative power of exclusion was ≥ 0.999929363 for both amplification systems in all populations. No significant departure from Hardy-Weinberg equilibrium was detected for D2S1338, D19S433, Penta D, and Penta E or the 13 Combined DNA Index System core STR loci after correction for multiple testing. Significant genetic diversity was observed between these four populations. Comparison with published frequency data for other populations is also presented.

Evidence for evolution in response to natural selection in a contemporary human population.

It is often claimed that modern humans have stopped evolving because cultural and technological advancements have annihilated natural selection. In contrast, recent studies show that selection can be strong in contemporary populations. However, detecting a response to selection is particularly challenging; previous evidence from wild animals has been criticized for both applying anticonservative statistical tests and failing to consider random genetic drift. Here we study life-history variation in an insular preindustrial French-Canadian population and apply a recently proposed conservative approach to testing microevolutionary responses to selection. As reported for other such societies, natural selection favored an earlier age at first reproduction (AFR) among women. AFR was also highly heritable and genetically correlated to fitness, predicting a microevolutionary change toward earlier reproduction. In agreement with this prediction, AFR declined from about 26-22 y over a 140-y period. Crucially, we uncovered a substantial change in the breeding values for this trait, indicating that the change in AFR largely occurred at the genetic level. Moreover, the genetic trend was higher than expected under the effect of random genetic drift alone. Our results show that microevolution can be detectable over relatively few generations in humans and underscore the need for studies of human demography and reproductive ecology to consider the role of evolutionary processes.

Physiological Dysregulation Proceeds and Predicts Health Outcomes Similarly in Chinese and Western Populations.

BACKGROUND: A decade ago, we proposed an index of physiological dysregulation based on Mahalanobis distance (DM) that measures how far from the norm an individual biomarker profile is. While extensive validation has been performed, focus was mostly on Western populations with little comparison to developing countries, particularly at a physiological system level. The degree to which the approach would work in other sociocultural contexts and the similarity of dysregulation signatures across diverse populations are still open questions. METHODS: Using 2 data sets from China and 3 from Western countries (United States, United Kingdom, and Italy), we calculated DM globally and per physiological system. We assessed pairwise correlations among systems, difference with age, prediction of mortality and age-related diseases, and sensitivity to interchanging data sets with one another as the reference in DM calculation. RESULTS: Overall, results were comparable across all data sets. Different physiological systems showed distinct dysregulation processes. Association with age was moderate and often nonlinear, similarly for all populations. Mahalanobis distance predicted most health outcomes, although differently by physiological system. Using a Chinese population as the reference when calculating DM for Western populations, or vice versa, led to similar associations with health outcomes, with a few exceptions. CONCLUSIONS: While small differences were noticeable, they did not systematically emerge between Chinese and Western populations, but rather diffusively across all data sets. These findings suggest that DM presents similar properties, notwithstanding sociocultural backgrounds, and that it is equally effective in capturing the loss of homeostasis that occurs during aging in diverse industrial human populations.

The effective family size of immigrant founders predicts their long-term demographic outcome: From Québec settlers to their 20th-century descendants.

Population history reconstruction, using extant genetic diversity data, routinely relies on simple demographic models to project the past through ascending genealogical-tree branches. Because genealogy and genetics are intimately related, we traced descending genealogies of the Québec founders to pursue their fate and to assess their contribution to the present-day population. Focusing on the female and male founder lines, we observed important sex-biased immigration in the early colony years and documented a remarkable impact of these early immigrants on the genetic make-up of 20th-century Québec. We estimated the immigrants' survival ratio as a proportion of lineages found in the 1931-60 Québec to their number introduced within the immigration period. We assessed the effective family size, EFS, of all immigrant parents and their Québec-born descendants. The survival ratio of the earliest immigrants was the highest and declined over centuries in association with the immigrants' EFS. Parents with high EFS left plentiful married descendants, putting EFS as the most important variable determining the parental demographic success throughout time for generations ahead. EFS of immigrant founders appears to predict their long-term demographic and, consequently, their genetic outcome. Genealogically inferred immigrants' "autosomal" genetic contribution to 1931-60 Québec from consecutive immigration periods follow the same yearly pattern as the corresponding maternal and paternal lines. Québec genealogical data offer much broader information on the ancestral diversity distribution than genetic scrutiny of a limited population sample. Genealogically inferred population history could assist studies of evolutionary factors shaping population structure and provide tools to target specific health interventions.

Genotype-by-environment interactions modulate the rate of microevolution in reproductive timing in humans.

Evidence from natural populations shows that changes in environmental conditions can cause rapid modifications in the evolutionary potential of phenotypes, partly through genotype-by-environment interactions (G×E). Therefore, the overall rate of microevolution should depend on fluctuations in environmental conditions, even when directional selection is sustained over several generations. We tested this hypothesis in a preindustrial human population that experienced a microevolutionary change in age at first reproduction (AFR) of mothers, using the annual infant mortality rate (IMR) as an indicator of environmental conditions during their early life. Using quantitative genetics analyses, we found that G×Es explained a nonnegligible fraction of the additive genetic variance in AFR and in relative fitness, as well as of the genetic covariance between AFR and fitness (i.e., the Robertson-Price covariance). The covariance was stronger for individuals exposed to unfavorable early-life environmental conditions. Our results unravel the presence of G×Es in an important life history trait and its impact on the rate of microevolution, which appears to have been sensitive to short-term fluctuations in local environmental conditions.

Determining the impact of unknown individuals in criminality using network analysis of DNA matches.

Criminal offenders missing from police files limit the capacity to reconstruct criminal networks for criminological research and operational purposes. Recent studies show that forensic DNA databanks offer potential to address this problem, through large-scale analysis of DNA matches, many of which involve unidentified offenders. Applying social network analysis (SNA) to 18 years of DNA match data from Québec, Canada, we found that 1400 unknowns do not occupy more marginal positions in the network than 13,000 known offenders, and explain up to 18% of SNA values (e.g., betweenness centrality) for the latter while supporting 46% of their clustering values. Our results contrast with previous studies, showing moreover that unknown individuals who are positioned centrally in a network may have a larger impact than previously expected on investigation policing with implications for forensic intelligence.

Small-scale dispersal and survival in a long-lived seabird, the wandering albatross.

1. Dispersal is a fundamental but still poorly known process in population dynamics and several hypotheses have been proposed to explain its patterns. We studied natal and breeding dispersal and survival in a long-lived seabird, the wandering albatross (Diomedea exulans L.), and examined several hypotheses concerning dispersal patterns in birds. 2. We applied multi-state capture-recapture models to a 36-year data set (1969-2004) collected at three albatross colonies on Ile de Possession, Crozet Islands. Because the species has biennial reproduction, we introduced unobservable states in the model to account for the absence of individuals in those years. 3. Adults were highly faithful to their nesting colony but colony fidelity, as well as survival rate, differed slightly among colonies (fidelity ranged from 0.957 to 0.977). Breeding fidelity was highest in the colony where survival was lowest and individuals were not more likely to change colony following a failed breeding attempt than after a successful one. The colony that attracted most dispersers had the lowest density of nesting birds. 4. Philopatry (the probability that young return to breed at a birth site) was generally high but variable among colonies (ranging from 0.70 to 0.92), and survival of young differed little. Philopatry was highest in the largest colony, where the availability of potential mates was presumably greatest. However, among dispersing individuals, the colony that had the lowest density of nesting individuals, not the largest colony, attracted the most recruits. 5. Although size of the colony influenced the decision to stay or to leave in young, density was most influential in the selection of a new colony among both adult and young dispersers. Our results support the hypothesis that philopatry is the strategy favoured by most recruits and that conspecific attraction can explain variation in the level of philopatry among colonies but not settlement patterns among dispersing individuals.

The dimensions of evolutionary potential in biological conservation.

It is now well admitted by ecologists that the conservation of biodiversity should imply preserving the evolutionary processes that will permit its adaptation to ongoing and future environmental changes. This is attested by the ever-growing reference to the conservation of evolutionary potential in the scientific literature. The impression that one may have when reading papers is that conserving evolutionary potential can only be a good thing, whatever biological system is under scrutiny. However, different objectives, such as maintaining species richness versus ecosystem services, may express different, when not conflicting, underlying values attributed to biodiversity. For instance, biodiversity can be intrinsically valued, as worth it to be conserved per se, or it can be conserved as a means for human flourishing. Consequently, both the concept of evolutionary potential and the prescriptions derived from the commitment to conserve it remain problematic, due to a lack of explicit mention of the norms underlying different conservation visions. Here, we contend that those who advocate for the conservation of evolutionary potential should position their conception along four dimensions: what vehicles instantiate the evolutionary potential relevant to their normative commitment; what temporality is involved; how measurable evolutionary potential is, and what degree of human influence is tolerated. We need to address these dimensions if we are to determine why and when the maintenance of evolutionary potential is an appropriate target for the conservation of biodiversity.

Must the random man be unrelated? A lingering misconception in forensic genetics.

A nearly universal practice among forensic DNA scientists includes mentioning an unrelated person as the possible alternative source of a DNA stain, when one in fact refers to an unknown person. Hence, experts typically express their conclusions with statements like: "The probability of the DNA evidence is X times higher if the suspect is the source of the trace than if another person unrelated to the suspect is the source of the trace." Published forensic guidelines encourage such allusions to the unrelated person. However, as the authors show here, rational reasoning and population genetic principles do not require the conditioning of the evidential value on the unrelatedness between the unknown individual and the person of interest (e.g., a suspect). Surprisingly, this important semantic issue has been overlooked for decades, despite its potential to mislead the interpretation of DNA evidence by criminal justice system stakeholders.

Tug of war between continental gene flow and rearing site philopatry in a migratory bird: the sex-biased dispersal paradigm reconsidered.

Nonrandom dispersal has been recently advanced as a mechanism promoting fine-scale genetic differentiation in resident populations, yet how this applies to species with high rates of dispersal is still unclear. Using a migratory species considered a classical example of male-biased dispersal (the greater snow goose, Chen caerulescens atlantica), we documented a temporally stable fine-scale genetic clustering between spatially distinct rearing sites (5-30 km apart), where family aggregates shortly after hatching. Such genetic differentiation can only arise if, in both sexes, dispersal is restricted and nonrandom, a surprising result considering that pairing occurs among mixed flocks of birds more than 3000 km away from the breeding grounds. Fine-scale genetic structure may thus occur even in migratory species with high gene flow. We further show that looking for genetic structure based on nesting sites only may be misleading. Genetically distinct individuals that segregated into different rearing sites were in fact spatially mixed during nesting. These findings provide new, scale-dependent links between genetic structure, pairing, and dispersal and show the importance of sampling different stages of the breeding cycle in order to detect a spatial genetic structure.

The seabird paradox: dispersal, genetic structure and population dynamics in a highly mobile, but philopatric albatross species.

The philopatric behaviour of albatrosses has intrigued biologists due to the high mobility of these seabirds. It is unknown how albatrosses maintain a system of fragmented populations without frequent dispersal movements, in spite of the long-term temporal heterogeneity in resource distribution at sea. We used both genetic (amplified fragment length polymorphism) and capture-mark-recapture (CMR) data to identify explicitly which among several models of population dynamics best applies to the wandering albatross (Diomedea exulans) and to test for migration-drift equilibrium. We previously documented an extremely low genetic diversity in this species. Here, we show that populations exhibit little genetic differentiation across the species' range (Theta(B) < 0.05, where Theta(B) is an F(ST) analogue). Furthermore, there was no evidence of hierarchical structure or isolation-by-distance. Wright's F(ST) between pairs of colonies were low in general and the pattern was consistent with a nonequilibrium genetic model. In contrast, CMR data collected over the last decades indicated that about one bird per cohort has dispersed among islands. Overall, F(ST) values were not indicative of contemporary dispersal as inferred from CMR data. Moreover, all genotypes grouped together in a cluster analysis, indicating that current colonies may have derived from one ancestral source that had a low genetic diversity. A metapopulation dynamics model including a recent (postglacial) colonization of several islands seems consistent with both the very low levels of genetic diversity and structure within the wandering albatross. Yet, our data suggest that several other factors including ongoing gene flow, recurrent long-distance dispersal and source-sink dynamics have contributed to different extent in shaping the genetic signature observed in this species. Our results show that an absence of genetic structuring may in itself reveal little about the true population dynamics in seabirds, but can provide insights into important processes when a comparison with other information, such as demographic data, is possible.

Surviving with low genetic diversity: the case of albatrosses.

Low genetic diversity is predicted to negatively impact species viability and has been a central concern for conservation. In contrast, the possibility that some species may thrive in spite of a relatively poor diversity has received little attention. The wandering and Amsterdam albatrosses (Diomedea exulans and Diomedea amsterdamensis) are long-lived seabirds standing at an extreme along the gradient of life strategies, having traits that may favour inbreeding and low genetic diversity. Divergence time of the two species is estimated at 0.84 Myr ago from cytochrome b data. We tested the hypothesis that both albatrosses inherited poor genetic diversity from their common ancestor. Within the wandering albatross, per cent polymorphic loci and expected heterozygosity at amplified fragment length polymorphisms were approximately one-third of the minimal values reported in other vertebrates. Genetic diversity in the Amsterdam albatross, which is recovering from a severe bottleneck, was about twice as low as in the wandering albatross. Simulations supported the hypothesis that genetic diversity in albatrosses was already depleted prior to their divergence. Given the generally high breeding success of these species, it is likely that they are not suffering much from their impoverished diversity. Whether albatrosses are unique in this regard is unknown, but they appear to challenge the classical view about the negative consequences of genetic depletion on species survival.

Mother's curse neutralizes natural selection against a human genetic disease over three centuries.

According to evolutionary theory, mitochondria could be poisoned gifts that mothers transmit to their sons. This is because mutations harmful to males are expected to accumulate in the mitochondrial genome, the so-called 'mother's curse'. However, the contribution of the mother's curse to the mutation load in nature remains largely unknown and hard to predict, because compensatory mechanisms could impede the spread of deleterious mitochondria. Here we provide evidence for the mother's curse in action over 290 years in a human population. We studied a mutation causing Leber's hereditary optical neuropathy, a disease with male-biased prevalence and which has long been suspected to be maintained in populations by the mother's curse. Male carriers showed a low fitness relative to non-carriers and to females, mostly explained by their high rate of infant mortality. Despite poor male fitness, selection analysis predicted a slight (albeit non-significant) increase in frequency, which sharply contrasts with the 35.5% per-generation decrease predicted if mitochondrial DNA transmission had been through males instead of females. Our results are therefore even suggestive of positive selection through the female line that may exacerbate effects of the mother's curse. This study supports a contribution of the mother's curse to the reduction of male lifespan, uncovering a large fitness effect associated with a single mitochondrial variant.

Eco-evolutionary dynamics in a contemporary human population.

Recent studies of the joint dynamics of ecological and evolutionary processes show that changes in genotype or phenotype distributions can affect population, community and ecosystem processes. Such eco-evolutionary dynamics are likely to occur in modern humans and may influence population dynamics. Here, we study contributions to population growth from detailed genealogical records of a contemporary human population. We show that evolutionary changes in women's age at first reproduction can affect population growth: 15.9% of variation in individual contribution to population growth over 108 years is explained by mean age at first reproduction and at least one-third of this variation (6.1%) is attributed to the genetic basis of this trait, which showed an evolutionary response to selection during the period studied. Our study suggests that eco-evolutionary processes have modulated the growth of contemporary human populations.

Optimal Versus Realized Trajectories of Physiological Dysregulation in Aging and Their Relation to Sex-Specific Mortality Risk.

While longitudinal changes in biomarker levels and their impact on health have been characterized for individual markers, little is known about how overall marker profiles may change during aging and affect mortality risk. We implemented the recently developed measure of physiological dysregulation based on the statistical distance of biomarker profiles in the framework of the stochastic process model of aging, using data on blood pressure, heart rate, cholesterol, glucose, hematocrit, body mass index, and mortality in the Framingham original cohort. This allowed us to evaluate how physiological dysregulation is related to different aging-related characteristics such as decline in stress resistance and adaptive capacity (which typically are not observed in the data and thus can be analyzed only indirectly), and, ultimately, to estimate how such dynamic relationships increase mortality risk with age. We found that physiological dysregulation increases with age; that increased dysregulation is associated with increased mortality, and increasingly so with age; and that, in most but not all cases, there is a decreasing ability to return quickly to baseline physiological state with age. We also revealed substantial sex differences in these processes, with women becoming dysregulated more quickly but with men showing a much greater sensitivity to dysregulation in terms of mortality risk.