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Benning, J. W.

Publications and source records attributed to Benning, J. W..

7 recordsLinked to original sources

Expansion load reduces fitness at the range margin of an invasive plant

Genetic drift and natural selection jointly shape how populations evolve during range expansion, yet their joint influence on fitness at expanding range margins is rarely examined. Serial founder events during range expansion may amplify genetic drift and result in the accumulation (or greater expression) of deleterious mutations at range margins, termed expansion load. Conversely, natural selection should lead to local adaptation during expansion provided that populations harbor adequate genetic variation. We used a manipulative transplant experiment, genome-wide SNP data, and demographic surveys of the invasive plant, commontansy (Tanacetum vulgare), to evaluate evidence for expansion load and local adaptation during ca. 150 years of invasion in Minnesota, U.S.A. The common garden occurred near the southern range margin and included 16 populations that span (1) a chronosequence of invasion from northeastern MN (invasion core) to southern and western range margins and (2) environmental gradients in temperature and precipitation. We also manipulated temperature and precipitation to test whether environmental stress amplified the expression of expansion load or revealed population differentiation in climate adaptation. Population fitness declined strongly with distance from the invasion core, consistent with the accumulation of expansion load. This finding was corroborated by analyses of 173 populations that showed an increase in homozygosity (F) and a decrease in population size from the invasion core to range margins. We did not find any evidence of local adaptation; a strong positive relationship between population mean fitness and environmental distance was indicative of maladaptation. While the elevated temperature manipulation reduced fitness, it did not amplify the expression of expansion load. Taken together, our results are consistent with the hypothesis that serial population bottlenecks and strong genetic drift led to expansion load and reduced fitness at range margins. Teaser TextSpecies geographic ranges are dynamic over geologic time scales but may also shift rapidly in response to climate change and for invasive species. While range shifts are often viewed only through an ecological lens, the extent and pace of range expansion may be significantly modulated by evolutionary processes. We disentangled the influence of genetic drift and natural selection on population fitness across an invasion chronosequence (spanning ca. 150 years) for the herbaceous plant common tansy (Tanacetum vulgare). Our synthesis of analyses of a field transplant experiment, genome-wide SNP data, and demographic surveys provided evidence consistent with the accumulation of expansion load at leading range edges. While theory often predicts that local adaptation should occur readily in response to novel environments, our results were consistent with local maladaptation. Our findings emphasize the importance of stochastic processes in shaping the geographic distribution of species and their capacity to shift with changing environments.

evolutionary biology↗

Environmental gradients mediate dispersal evolution during biological invasions

Rapid dispersal evolution at the edge of a range expansion can accelerate invasions. However, expanding populations will often encounter environmental gradients that entail a fitness cost of dispersal. We used an eco-evolutionary model to explore how environmental heterogeneity influences adaptation and dispersal evolution during range expansion and, in turn, modulates the speed and predictability of invasion. Environmental gradients opposed the evolution of increased dispersal during invasion, even leading to the evolution of reduced dispersal along steep gradients. Counterintuitively, reduced dispersal allowed for faster expansion by minimizing maladaptation. While evolution across homogenous landscapes caused invasions to be highly unpredictable, even shallow environmental gradients greatly increased invasion predictability. We illustrate our models potential application to prediction and management of invasions by parameterizing it with data from a recent invertebrate range expansion. Overall, we find that environmental heterogeneity and local adaptation strongly modulate the effect of dispersal evolution on invasion trajectories.

ecology↗

Clark (2023) and the Persistence of Hereditarian Fallacies

The scientific literature has seen a resurgence of interest in genetic influences on human behavior and socioeconomic outcomes. Such studies face the central difficulty of distinguishing possible causal influences, in particular genetic and non-genetic ones. When confounding between possible influences is not rigorously addressed, it invites over- and misinterpretation of data. We illustrate the breadth of this problem through a discussion of the literature and a reanalysis of two examples. Clark (2023) suggested that patterns of similarity in social status between relatives indicate that social status is largely determined by ones DNA. We show that the papers conclusions are based on the conflation of genetic and non-genetic transmission (for example, of wealth) within families. Song & Zhang (2024) posited that genetic variants underlying bisexual behavior are maintained in the population because they also affect risk-taking behavior, thereby conferring an evolutionary fitness advantage through increased sexual promiscuity. In this case, too, we show that possible explanations cannot be distinguished, but only one is chosen and presented as a conclusion. We discuss how issues of confounding apply more broadly to studies that claim to establish genetic underpinnings to human behavior and societal outcomes.

genetics↗

Rapid evolution in response to climate-change-induced drought and its demographic and genetic controls

Populations often vary in their evolutionary responses to a shared environmental perturbation. A key hurdle in building more predictive models of rapid evolution is understanding this variation - why do some populations and traits evolve while others do not? We combined long-term demographic and environmental data, estimates of quantitative genetic variance components, a resurrection experiment, and individual-based evolutionary simulations to gain mechanistic insights into contrasting evolutionary responses to a severe multiyear drought. We examined five traits in two populations of a native California plant, Clarkia xantiana, at three timepoints over 7 years. Earlier flowering phenology evolved in only one of the two populations, though both populations experienced similar drought severity and demographic declines and were estimated to have considerable additive genetic variance for flowering phenology. Pairing demographic and experimental data with evolutionary simulations suggested that while seed banks in both populations likely constrained evolutionary responses, a stronger seed bank in the non-evolving population resulted in evolutionary stasis. Gene flow through time via germ banks may be an important, underappreciated control on rapid evolution in response to extreme environmental perturbations.

evolutionary biology↗

The spatial scale of adaptation in a native annual plant and its implications for responses to climate change

Spatial patterns of adaptation provide important insights into agents of selection and expected responses of populations to climate change. Robust inference into the spatial scale of adaptation can be gained through reciprocal transplant experiments that combine multiple source populations and common gardens. Here we examine the spatial scale of local adaptation of the North American annual plant common ragweed, Ambrosia artemisiifolia, using data from four common gardens with 22 source populations sampled from across a [~]1200 km latitudinal gradient within the native range. We found evidence of local adaptation at the northernmost common garden, but maladaptation at the two southern gardens, where more southern source populations outperformed local populations. Overall, the spatial scale of adaptation was large -- at the three gardens where distance between source populations and gardens explained variation in fitness, it took an average of 820 km for fitness to decline to 50% of its predicted maximum. Taken together, these results suggest that climate change has already caused maladaptation, especially across the southern portion of the range, and may result in northward range contraction over time.

evolutionary biology↗

Increasing temporal variance leads to stable species range limits

What prevents populations of a species from adapting to the novel environments outside the species geographic distribution? Previous models highlighted how gene flow across spatial environmental gradients determines species expansion vs. extinction and the location of species range limits. However, space is only one of two axes of environmental variation -- environments also vary in time, and we know temporal environmental variation has important consequences for population demography and evolution. We used analytical and individual-based evolutionary models to explore how temporal variation in environmental conditions influences the spread of populations across a spatial environmental gradient. We find that temporal variation greatly alters our predictions for range dynamics compared to temporally static environments. When temporal variance is equal across the landscape, the fate of species (expansion vs. extinction) is determined by the interaction between the degree of temporal autocorrelation in environmental fluctuations and the steepness of the spatial environmental gradient. When the magnitude of temporal variance changes across the landscape, stable range limits form where this variance increases maladaptation sufficiently to prevent local persistence. These results illustrate the pivotal influence of temporal variation on the likelihood of populations colonizing novel habitats and the location of species range limits.

evolutionary biology↗

Seed predation increases from the Arctic to the Equator and from high to low elevations

Species interactions have long been predicted to increase in intensity towards the tropics and low elevations, due to gradients in climate, productivity, or biodiversity. Despite their importance for understanding global ecological and evolutionary processes, plant-animal interaction gradients are particularly difficult to test systematically across large geographic gradients, and evidence from smaller, disparate studies is inconclusive. By systematically measuring post-dispersal seed predation using 6980 standardized seed depots along 18 mountains in the Pacific cordillera, we found that seed predation increases 18% from the Arctic to Equator and 16% from 4000 masl to sea level. Clines in total predation, likely driven by invertebrates, were consistent across tree-line ecotones and in continuous forest, and were better explained by climate seasonality than by productivity, biodiversity, or latitude. These results suggest that species interactions play predictably greater ecological and evolutionary roles in tropical, lowland, and other less seasonal ecosystems.\n\nOne Sentence SummaryPost-dispersal seed predation increases from the Arctic to the Equator and from high elevations to sea level.

ecology↗