The relationship between neutral genetic diversity and performance in wild arthropod populations.

Larger effective populations (Ne) are characterized by higher genetic diversity, which is expected to predict population performance (average individual performance that influences fitness). Empirical studies of the relationship between neutral diversity and performance mostly represent species with small Ne, while there is limited data from the species-rich and ecologically important arthropods that are assumed to have large Ne but are threatened by massive declines. We performed a systematic literature search and used meta-analytical models to test the prediction of a positive association between neutral genetic diversity and performance in wild arthropods. From 14 relevant studies of 286 populations, we detected a weak (r = 0.15) but nonsignificant positive association both in the full data set (121 effect sizes) and a reduced data set accounting for dependency (14 effect sizes). Theory predicts that traits closely associated with fitness show a relatively stronger correlation with neutral diversity; this relationship was upheld for longevity and marginally for reproduction. Our analyses point to major knowledge gaps in our understanding of relationships between neutral diversity and performance. Future studies using genome-wide data sets across populations could guide more powerful designs to evaluate relationships between adaptive, deleterious and neutral diversity and performance.

Extent of intraspecific trait variability in ecologically central and marginal populations of a dominant alpine plant across European mountains.

BACKGROUND AND AIMS: Studying trait variability and restricted gene flow between populations of species can reveal species dynamics. Peripheral populations commonly exhibit lower genetic diversity and trait variability due to isolation and ecological marginality, unlike central populations experiencing gene flow and optimal conditions. This study focused on Carex curvula, the dominant species in alpine acidic meadows of European mountain regions. The species is sparser in dry areas such as the Pyrenees and Balkans, compared to the Central-Eastern Alps and Carpathians. We hypothesized that distinct population groups could be identified based on their mean functional trait values and their correlation with the environment; we predicted that ecologically marginal populations would have stronger trait correlations, lower within-population trait variability (intraspecific trait variability, ITV) and lower genetic diversity than populations of optimal habitats. METHODS: Sampling was conducted in 34 populations that spanned the entire distribution range of C. curvula. We used hierarchical clustering to identify emergent functional groups of populations, defined by combinations of multiple traits associated with nutrient economy and drought tolerance (e.g. specific leaf area, anatomy). We contrasted the geographical distribution of these groups in relation to environment and genetic structure. We compared pairwise trait relationships, within-population trait variation (ITV) and neutral genetic diversity between groups. KEY RESULTS: Our study identified emergent functional groups of populations. Those in the southernmost ranges, specifically the Pyrenees and Balkan region, showed drought-tolerant trait syndromes and correlated with indicators of limited water availability. While we noted a decline in population genetic diversity, we did not observe any significant changes in ITV in ecologically marginal (peripheral) populations. CONCLUSIONS: Our research exemplifies the relationship between ecological marginality and geographical peripherality, which in this case study is linked to genetic depauperation but not to reduced ITV. Understanding these relationships is crucial for understanding the biogeographical factors shaping trait variation.

Life history traits and dispersal shape neutral genetic diversity in metapopulations.

Genetic diversity at population scale, depends on species life-history traits, population dynamics and local and global environmental factors. We first investigate the effect of life-history traits on the neutral genetic diversity of a single population using a deterministic mathematical model. When the population is stable, we show that semelparous species with precocious maturation and iteroparous species with delayed maturation exhibit higher diversity because their life history traits tend to balance the lifetimes of non reproductive individuals (juveniles) and adults which reproduce. Then, we extend our model to a metapopulation to investigate the additional effect of dispersal on diversity. We show that dispersal may truly modify the local effect of life history on diversity. As a result, the diversity at the global scale of the metapopulation differ from the local diversity which is only described through local life history traits of the populations. In particular, dispersal usually promotes diversity at the global metapopulation scale.

Genealogical structure changes as range expansions transition from pushed to pulled.

Range expansions accelerate evolution through multiple mechanisms, including gene surfing and genetic drift. The inference and control of these evolutionary processes ultimately rely on the information contained in genealogical trees. Currently, there are two opposing views on how range expansions shape genealogies. In invasion biology, expansions are typically approximated by a series of population bottlenecks producing genealogies with only pairwise mergers between lineages-a process known as the Kingman coalescent. Conversely, traveling wave models predict a coalescent with multiple mergers, known as the Bolthausen-Sznitman coalescent. Here, we unify these two approaches and show that expansions can generate an entire spectrum of coalescent topologies. Specifically, we show that tree topology is controlled by growth dynamics at the front and exhibits large differences between pulled and pushed expansions. These differences are explained by the fluctuations in the total number of descendants left by the early founders. High growth cooperativity leads to a narrow distribution of reproductive values and the Kingman coalescent. Conversely, low growth cooperativity results in a broad distribution, whose exponent controls the merger sizes in the genealogies. These broad distribution and non-Kingman tree topologies emerge due to the fluctuations in the front shape and position and do not occur in quasi-deterministic simulations. Overall, our results show that range expansions provide a robust mechanism for generating different types of multiple mergers, which could be similar to those observed in populations with strong selection or high fecundity. Thus, caution should be exercised in making inferences about the origin of non-Kingman genealogies.

Dispersal and Good Habitat Quality Promote Neutral Genetic Diversity in Metapopulations.

Dispersal is a fundamental and crucial ecological process for a metapopulation to survive in heterogeneous or changing habitats. In this paper, we investigate the effect of the habitat quality and the dispersal on the neutral genetics diversity of a metapopulation. We model the metapopulation dynamics on heterogeneous habitats using a deterministic system of ordinary differential equations. We decompose the metapopulation into several neutral genetic fractions seeing as they could be located in different habitats. By using a mathematical model which describes their temporal dynamics inside the metapopulation, we provide the analytical results of their transient dynamics, as well as their asymptotic proportion in the different habitats. The diversity indices show how the genetic diversity at a global metapopulation scale is preserved by the correlation of two factors: the dispersal of the population, as well as the existence of adequate and sufficiently large habitats. The diversity indices show how the genetic diversity at a global metapopulation scale is preserved by the correlation of two factors: the dispersal of the population as well as the existence of adequate and sufficiently large habitats. Moreover, they ensure genetic diversity at the local habitat scale. In a source-sink metapopulation, we demonstrate that the diversity of the sink can be rescued if the condition of the sink is not too deteriorated and the migration from the source is larger than the migration from the sink. Furthermore, our study provides an analytical insight into the dynamics of the solutions of the systems of ordinary differential equations.

Using environmental and geographic data to optimize ex situ collections and preserve evolutionary potential.

Maintenance of biodiversity through seed banks and botanical gardens, where the wealth of species' genetic variation may be preserved ex situ, is a major goal of conservation. However, challenges can persist in optimizing ex situ collections if trade-offs exist among cost, effort, and conserving species evolutionary potential, particularly when genetic data are not available. We evaluated the genetic consequences of population preservation informed by geographic (isolation by distance [IBD]) and environmental (isolation by environment [IBE]) distance for ex situ collections for which population provenance is available. We used 19 genetic and genomic data sets from 15 plant species to assess the proportion of population genetic differentiation explained by geographic and environmental factors and to simulate ex situ collections prioritizing source populations based on pairwise geographic distance, environmental distance, or both. Specifically, we tested the impact prioritizing sampling based on these distances may have on the capture of neutral, functional, or putatively adaptive genetic diversity and differentiation. Individually, IBD and IBE explained limited population genetic differences across all 3 genetic marker classes (IBD, 10-16%; IBE, 1-5.5%). Together, they explained a substantial proportion of population genetic differences for functional (45%) and adaptive (71%) variation. Simulated ex situ collections revealed that inclusion of IBD, IBE, or both increased allelic diversity and genetic differentiation captured among populations, particularly for loci that may be important for adaptation. Thus, prioritizing population collections based on environmental and geographic distance data can optimize genetic variation captured ex situ. For the vast majority of plant species for which there is no genetic information, these data are invaluable to conservation because they can guide preservation of genetic variation needed to maintain evolutionary potential within collections.

Uso de Datos Ambientales y Geográficos para Optimizar las Colecciones Ex Situ y Preservar el Potencial Evolutivo Resumen El mantenimiento de la biodiversidad por medio de bancos de semillas y jardines botánicos, en donde la riqueza de la variación genética de las especies puede preservarse ex situ, es una de las principales metas de la conservación. Sin embargo, los obstáculos para la optimización de las colecciones ex situ pueden persistir si existen compensaciones entre el costo, el esfuerzo y la conservación del potencial evolutivo de la especie, particularmente cuando no están disponibles los datos genéticos. Evaluamos las consecuencias genéticas que tiene la preservación de una población fundamentada en la distancia geográfica (aislamiento por distancia [APD]) y ambiental (aislamiento por entorno [APE]) para las colecciones ex situ cuyo origen poblacional está disponible. Usamos 19 conjuntos de datos genéticos y genómicos de 15 especies de plantas para evaluar la proporción de la diferenciación genética de la población explicada por los factores geográficos y ambientales y para simular las colecciones ex situ que priorizan a las poblaciones de origen con base en la distancia geográfica por pares, la distancia ambiental, o ambas. Específicamente, comprobamos el impacto que puede tener la priorización de muestreos basados en estas distancias sobre la captura de la diferenciación y la diversidad genética neutral, funcional o putativamente adaptativa. De manera individual, el APD y el APE explicaron las diferencias limitadas en la genética poblacional en todas las clases de marcadores genéticos (APD, 10-16%; APE, 1-5.5%). En conjunto, ambos tipos de aislamiento explicaron una proporción sustancial de las diferencias en la genética poblacional para la variación funcional (45%) y adaptativa (71%). La simulación de colecciones ex situ reveló que la inclusión del APD, APE o ambos incrementó la diversidad de alelos y la diferenciación genética capturada entre las poblaciones, particularmente para los loci que pueden ser importantes para la adaptación. Por lo tanto, la priorización de las colecciones poblacionales basadas en los datos de distancia geográfica o ambiental pueden optimizar la variación genética capturada ex situ. Para la mayoría de las especies de plantas para las cuales no hay información genética, estos datos son indispensables para la conservación porque pueden dirigir la preservación de la variación genética necesaria para mantener el potencial evolutivo dentro de las colecciones.

The impact of long-range dispersal on gene surfing.

Range expansions lead to distinctive patterns of genetic variation in populations, even in the absence of selection. These patterns and their genetic consequences have been well studied for populations advancing through successive short-ranged migration events. However, most populations harbor some degree of long-range dispersal, experiencing rare yet consequential migration events over arbitrarily long distances. Although dispersal is known to strongly affect spatial genetic structure during range expansions, the resulting patterns and their impact on neutral diversity remain poorly understood. Here, we systematically study the consequences of long-range dispersal on patterns of neutral variation during range expansion in a class of dispersal models which spans the extremes of local (effectively short-ranged) and global (effectively well-mixed) migration. We find that sufficiently long-ranged dispersal leaves behind a mosaic of monoallelic patches, whose number and size are highly sensitive to the distribution of dispersal distances. We develop a coarse-grained model which connects statistical features of these spatial patterns to the evolution of neutral diversity during the range expansion. We show that growth mechanisms that appear qualitatively similar can engender vastly different outcomes for diversity: Depending on the tail of the dispersal distance distribution, diversity can be either preserved (i.e., many variants survive) or lost (i.e., one variant dominates) at long times. Our results highlight the impact of spatial and migratory structure on genetic variation during processes as varied as range expansions, species invasions, epidemics, and the spread of beneficial mutations in established populations.

Inside Dynamics of Integrodifference Equations with Mutations.

The method of inside dynamics provides a theory that can track the dynamics of neutral gene fractions in spreading populations. However, the role of mutations has so far been absent in the study of the gene flow of neutral fractions via inside dynamics. Using integrodifference equations, we develop a neutral genetic mutation model by extending a previously established scalar inside dynamics model. To classify the mutation dynamics, we define a mutation class as the set of neutral fractions that can mutate into one another. We show that the spread of neutral genetic fractions is dependent on the leading edge of population as well as the structure of the mutation matrix. Specifically, we show that the neutral fractions that contribute to the spread of the population must belong to the same mutation class as the neutral fraction found in the leading edge of the population. We prove that the asymptotic proportion of individuals at the leading edge of the population spread is given by the dominant right eigenvector of the associated mutation matrix, independent of growth and dispersal parameters. In addition, we provide numerical simulations to demonstrate our mathematical results, to extend their generality and to develop new conjectures about our model.

Impact of demography on linked selection in two outcrossing Brassicaceae species.

Genetic diversity is shaped by mutation, genetic drift, gene flow, recombination, and selection. The dynamics and interactions of these forces shape genetic diversity across different parts of the genome, between populations and species. Here, we have studied the effects of linked selection on nucleotide diversity in outcrossing populations of two Brassicaceae species, Arabidopsis lyrata and Capsella grandiflora, with contrasting demographic history. In agreement with previous estimates, we found evidence for a modest population size expansion thousands of generations ago, as well as efficient purifying selection in C. grandiflora. In contrast, the A. lyrata population exhibited evidence for very recent strong population size decline and weaker efficacy of purifying selection. Using multiple regression analyses with recombination rate and other genomic covariates as explanatory variables, we can explain 47% of the variance in neutral diversity in the C. grandiflora population, while in the A. lyrata population, only 11% of the variance was explained by the model. Recombination rate had a significant positive effect on neutral diversity in both species, suggesting that selection at linked sites has an effect on patterns of neutral variation. In line with this finding, we also found reduced neutral diversity in the vicinity of genes in the C. grandiflora population. However, in A. lyrata no such reduction in diversity was evident, a finding that is consistent with expectations of the impact of a recent bottleneck on patterns of neutral diversity near genes. This study thus empirically demonstrates how differences in demographic history modulate the impact of selection at linked sites in natural populations.

Integrodifference equations in the presence of climate change: persistence criterion, travelling waves and inside dynamics.

To understand the effects that the climate change has on the evolution of species as well as the genetic consequences, we analyze an integrodifference equation (IDE) models for a reproducing and dispersing population in a spatio-temporal heterogeneous environment described by a shifting climate envelope. Our analysis on the IDE focuses on the persistence criterion, travelling wave solutions, and the inside dynamics. First, the persistence criterion, characterizing the global dynamics of the IDE, is established in terms of the basic reproduction number. In the case of persistence, a unique travelling wave is found to govern the global dynamics. The effects of the size and the shifting speed of the climate envelope on the basic reproduction number, and hence, on the persistence criterion, are also investigated. In particular, the critical domain size and the critical shifting speed are found in certain cases. Numerical simulations are performed to complement the theoretical results. In the case of persistence, we separate the travelling wave and general solutions into spatially distinct neutral fractions to study the inside dynamics. It is shown that each neutral genetic fraction rearranges itself spatially so as to asymptotically achieve the profile of the travelling wave. To measure the genetic diversity of the population density we calculate the Shannon diversity index and related indices, and use these to illustrate how diversity changes with underlying parameters.

Neutral Genetic Patterns for Expanding Populations with Nonoverlapping Generations.

We investigate the inside dynamics of solutions to integrodifference equations to understand the genetic consequences of a population with nonoverlapping generations undergoing range expansion. To obtain the inside dynamics, we decompose the solution into neutral genetic components. The inside dynamics are given by the spatiotemporal evolution of the neutral genetic components. We consider thin-tailed dispersal kernels and a variety of per capita growth rate functions to classify the traveling wave solutions as either pushed or pulled fronts. We find that pulled fronts are synonymous with the founder effect in population genetics. Adding overcompensation to the dynamics of these fronts has no impact on genetic diversity in the expanding population. However, growth functions with a strong Allee effect cause the traveling wave solution to be a pushed front preserving the genetic variation in the population. In this case, the contribution of each neutral fraction can be computed by a simple formula dependent on the initial distribution of the neutral fractions, the traveling wave solution, and the asymptotic spreading speed.

Expansion Under Climate Change: The Genetic Consequences.

Range expansion and range shifts are crucial population responses to climate change. Genetic consequences are not well understood but are clearly coupled to ecological dynamics that, in turn, are driven by shifting climate conditions. We model a population with a deterministic reaction-diffusion model coupled to a heterogeneous environment that develops in time due to climate change. We decompose the resulting travelling wave solution into neutral genetic components to analyse the spatio-temporal dynamics of its genetic structure. Our analysis shows that range expansions and range shifts under slow climate change preserve genetic diversity. This is because slow climate change creates range boundaries that promote spatial mixing of genetic components. Mathematically, the mixing leads to so-called pushed travelling wave solutions. This mixing phenomenon is not seen in spatially homogeneous environments, where range expansion reduces genetic diversity through gene surfing arising from pulled travelling wave solutions. However, the preservation of diversity is diminished when climate change occurs too quickly. Using diversity indices, we show that fast expansions and range shifts erode genetic diversity more than slow range expansions and range shifts. Our study provides analytical insight into the dynamics of travelling wave solutions in heterogeneous environments.