The field of landscape genetics has been rapidly evolving, adopting and adapting analytical frameworks to address research questions. Current studies are increasingly using regression‐based ...frameworks to infer the individual contributions of landscape and habitat variables on genetic differentiation. This paper outlines appropriate and inappropriate uses of multiple regression for these purposes, and demonstrates through simulation the limitations of different analytical frameworks for making correct inference. Of particular concern are recent studies seeking to explain genetic differences by fitting regression models with effective distance variables calculated independently on separate landscape resistance surfaces. When moving across the landscape, organisms cannot respond independently and uniquely to habitat and landscape features. Analyses seeking to understand how landscape features affect gene flow should model a single conductance or resistance surface as a parameterized function of relevant spatial covariates, and estimate the values of these parameters by linking a single set of resistance distances to observed genetic dissimilarity via a loss function. While this loss function may involve a regression‐like step, the associated nuisance parameters are not interpretable in terms of organismal movement and should not be conflated with what is actually of interest: the mapping between spatial covariates and conductance/resistance. The growth and evolution of landscape genetics as a field has been rapid and exciting. It is the goal of this paper to highlight past missteps and demonstrate limitations of current approaches to ensure that future use of regression models will appropriately consider the process being modeled, which will provide clarity to model interpretation.
Animal pollination mediates both reproduction and gene flow for the majority of plant species across the globe. However, past functional studies have focused largely on seed production; although ...useful, this focus on seed set does not provide information regarding species-specific contributions to pollen-mediated gene flow. Here we quantify pollen dispersal for individual pollinator species across more than 690 ha of tropical forest. Specifically, we examine visitation, seed production, and pollen-dispersal ability for the entire pollinator community of a common tropical tree using a series of individual-based pollinator-exclusion experiments followed by molecular-based fractional paternity analyses. We investigate the effects of pollinator body size, plant size (as a proxy of floral display), local plant density, and local plant kinship on seed production and pollen-dispersal distance. Our results show that while large-bodied pollinators set more seeds per visit, small-bodied bees visited flowers more frequently and were responsible for more than 49% of all long-distance (beyond 1 km) pollen-dispersal events. Thus, despite their size, small-bodied bees play a critical role in facilitating long-distance pollen-mediated gene flow. We also found that both plant size and local plant kinship negatively impact pollen dispersal and seed production. By incorporating genetic and trait-based data into the quantification of pollination services, we highlight the diversity in ecological function mediated by pollinators, the influential role that plant and population attributes play in driving service provision, and the unexpected importance of small-bodied pollinators in the recruitment of plant genetic diversity.
The expansion of agriculture is responsible for the mass conversion of biologically diverse natural environments into managed agroecosystems dominated by a handful of genetically homogeneous crop ...species. Agricultural ecosystems typically have very different abiotic and ecological conditions from those they replaced and create potential niches for those species that are able to exploit the abundant resources offered by crop plants. While there are well-studied examples of crop pests that have adapted into novel agricultural niches, the impact of agricultural intensification on the evolution of crop mutualists such as pollinators is poorly understood. We combined genealogical inference from genomic data with archaeological records to demonstrate that the Holocene demographic history of a wild specialist pollinator of
(pumpkins, squashes, and gourds) has been profoundly impacted by the history of agricultural expansion in North America. Populations of the squash bee
experienced rapid growth in areas where agriculture intensified within the past 1,000 y, suggesting that the cultivation of
in North America has increased the amount of floral resources available to these bees. In addition, we found that roughly 20% of this bee species' genome shows signatures of recent selective sweeps. These signatures are overwhelmingly concentrated in populations from eastern North America where squash bees were historically able to colonize novel environments due to human cultivation of
and now exclusively inhabit agricultural niches. These results suggest that the widespread cultivation of crops can prompt adaptation in wild pollinators through the distinct ecological conditions imposed by agricultural environments.
Abstract
Stochastic simulation is a key tool in population genetics, since the models involved are often analytically intractable and simulation is usually the only way of obtaining ground-truth data ...to evaluate inferences. Because of this, a large number of specialized simulation programs have been developed, each filling a particular niche, but with largely overlapping functionality and a substantial duplication of effort. Here, we introduce msprime version 1.0, which efficiently implements ancestry and mutation simulations based on the succinct tree sequence data structure and the tskit library. We summarize msprime’s many features, and show that its performance is excellent, often many times faster and more memory efficient than specialized alternatives. These high-performance features have been thoroughly tested and validated, and built using a collaborative, open source development model, which reduces duplication of effort and promotes software quality via community engagement.
Since its introduction in 2016, the msprime simulator has grown in popularity and is now one of the most commonly used tools in population genetics. This article marks the 1.0 release of msprime and summarizes the many features it has accumulated through an open source community development model. Despite its generality, msprime’s performance is excellent—in many cases orders of magnitude faster and more memory efficient than more specialized methods.
Ecological differentiation and genetic isolation are thought to be critical in facilitating coexistence between related species, but the relative importance of these phenomena and the interactions ...between them are not well understood. Here, we examine divergence in abiotic habitat affinity and the extent of hybridization and introgression between two rare species of Monardella (Lamiaceae) that are both restricted to the same serpentine soil exposure in California. Although broadly sympatric, they are found in microhabitats that differ consistently in soil chemistry, slope, rockiness and vegetation. We identify one active hybrid zone at a site with intermediate soil and above‐ground characteristics, and we document admixture patterns indicative of extensive and asymmetric introgression from one species into the other. We find that genetic distance among heterospecific populations is related to geographic distance, such that the extent of apparent introgression is partly explained by the spatial proximity to the hybrid zone. Our work shows that plant species can maintain morphological and ecological integrity in the face of weak genetic isolation, intermediate habitats can facilitate the establishment of hybrids, and that the degree of apparent introgression a population experiences is related to its geographic location rather than its local habitat characteristics.
A knowledge of the distances regularly travelled by foraging bees is essential to understanding the movement of pollen across landscapes, and has implications for the conservation of both pollinators ...and plants. Unfortunately, the movements of bees are difficult to measure directly at ecologically relevant scales. A common strategy for quantifying the foraging ranges of social bees is to sample the genotypes of foragers across a landscape. Individual foragers can be assigned to colonies with polymorphic genetic markers, and the dispersion of siblings in space can be used to make inference about colony locations and foraging movements. Several previous studies have sampled sibling genotypes at discrete locations (for example, at regular points along a transect), rather than in continuous space. Restricting the collection of bees to discrete locations presents a number of considerations for sampling design and data analysis. In this paper, we develop a spatially-explicit, model-based framework for the simulation and estimation of foraging ranges. Using these tools, we simulated experiments to characterise the efficacy of different sampling strategies, and provide an example with actual data that demonstrates the advantages of our method over an approach based on regression.
Abstract The genus Bombus (bumble bees) includes approximately 265 species, many of which are in decline in North America and Europe. To estimate colony abundance of bumble bees in natural and ...agricultural habitats, sibship relationships are often reconstructed from genetic data with the assumption that colonies have 1 monandrous queen. However, some species such as the North American common eastern bumble bee (Bombus impatiens Cresson) can display low levels of polyandry, which may bias estimates of colony abundance based on monandrous sibship reconstructions. To accurately quantify rates of polyandry in wild and commercially mated queens of this species, we empirically estimated mating frequencies using a novel statistical model and genotypes from 730 bees. To genotype individuals, we used a highly polymorphic set of microsatellites on colonies established from 20 wild-caught gynes and 10 commercial colonies. We found multiple fathers in 3 of the wild colonies and 3 of the commercial colonies. This resulted in average effective mating frequencies of 1.075 ± 0.18 and 1.154 ± 0.25 for wild and commercial colonies, respectively. These findings agree with previous reports of low rates of polyandry for B. impatiens. Using a large empirical dataset, we demonstrate that assuming monandry for colony abundance estimation in species that violate this assumption results in an overestimation of the number of colonies. Our results emphasize the importance of studying mating frequencies in social species of conservation concern and economic importance for the accuracy of colony abundance estimation and for understanding their ecology and sociobiology.
Although genetic diversity ultimately determines the ability of organisms to adapt to environmental changes, conservation assessments like the widely used International Union for Conservation of ...Nature (IUCN) Red List Criteria do not explicitly consider genetic information. Including a genetic dimension into the IUCN Red List Criteria would greatly enhance conservation efforts, because the demographic parameters traditionally considered are poor predictors of the evolutionary resilience of natural populations to global change. Here we perform the first genomic assessment of genetic diversity, gene flow, and patterns of local adaptation in tropical plant species belonging to different IUCN Red List Categories. Employing RAD-sequencing we identified tens of thousands of single-nucleotide polymorphisms in an endangered narrow-endemic and a least concern widespread morning glory (Convolvulaceae) from Amazonian savannas, a highly threatened and under-protected tropical ecosystem. Our results reveal greater genetic diversity and less spatial genetic structure in the endangered species. Whereas terrain roughness affected gene flow in both species, forested and mining areas were found to hinder gene flow in the endangered plant. Finally we implemented environmental association tests and genome scans for selection, and identified a higher proportion of candidate adaptive loci in the widespread species. These mainly contained genes related to pathogen resistance and physiological adaptations to life in nutrient-limited environments. Our study emphasizes that IUCN Red List Criteria do not always prioritize species with low genetic diversity or whose genetic variation is being affected by habitat loss and fragmentation, and calls for the inclusion of genetic information into conservation assessments. More generally, our study exemplifies how landscape genomic tools can be employed to assess the status, threats and adaptive responses of imperiled biodiversity.
Estimating population density and identifying those areas where density is changing through time are central to prioritizing conservation and management strategies. Obtaining reliable estimates of ...density and trends can be challenging, however, especially for long‐lived species that are rare, have broad geographic distributions, and are difficult to detect reliably during field surveys. We developed a hierarchical model for distance‐sampling data that characterizes spatial variation in density at two scales and simultaneously estimates regional trends while accounting for variation in detection probability and availability across surveys. We applied the model to data collected over a 20‐year period (2001–2020) in an area that encompassed most of the geographic range of the Mojave desert tortoise (Gopherus agassizii). Density of adult tortoises varied with multiple biotic and abiotic features, including topography, aspect, geology, and seasonal precipitation and temperature regimes. Across the entire period and study area, the density of adult tortoises decreased by an average of 1.8% per year (95% CI = −3.5% to −0.2%). Trends varied geographically, however, with the steepest declines in the western part of the range (−4.1%, −6.9% to −1.3%). Accounting for habitat loss across our study area, the abundance of this threatened species declined by an estimated 129,000 adults (36%) between 2001 and 2020. Our modeling approach extends traditional distance‐sampling frameworks by accounting for ecological and observational processes that could mask spatiotemporal variation in density and, at the same time, provides spatially explicit estimates to guide conservation and management strategies for tortoises and other rare species.
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