skip to main content

Attention:

The NSF Public Access Repository (NSF-PAR) system and access will be unavailable from 11:00 PM ET on Thursday, June 13 until 2:00 AM ET on Friday, June 14 due to maintenance. We apologize for the inconvenience.


Title: Patterns of genetic differentiation in Colorado potato beetle correlate with contemporary, not historic, potato land cover
Abstract

Changing landscape heterogeneity can influence connectivity and alter genetic variation in local populations, but there can be a lag between ecological change and evolutionary responses. Temporal lag effects might be acute in agroecosystems, where land cover has changed substantially in the last two centuries. Here, we evaluate how patterns of an insect pest’s genetic differentiation are related to past and present agricultural land cover change over a 150‐year period. We quantified change in the amount of potato,Solanum tuberosumL., land cover since 1850 using county‐level agricultural census reports, obtained allele frequency data from 7,408 single‐nucleotide polymorphism loci, and compared effects of historic and contemporary landscape connectivity on genetic differentiation of Colorado potato beetle,Leptinotarsa decemlineataSay, in two agricultural landscapes in the United States. We found that potato land cover peaked in Wisconsin in the early 1900s, followed by rapid decline and spatial concentration, whereas it increased in amount and extent in the Columbia Basin of Oregon and Washington beginning in the 1960s. In both landscapes, we found small effect sizes of landscape resistance on genetic differentiation, but a 20× to 1,000× larger effect of contemporary relative to historic landscape resistances. Demographic analyses suggest population size trajectories were largely consistent among regions and therefore are not likely to have differentially impacted the observed patterns of population structure in each region. Weak landscape genetic associations might instead be related to the coarse resolution of our historical land cover data. Despite rapid changes in agricultural landscapes over the last two centuries, genetic differentiation amongL. decemlineatapopulations appears to reflect ongoing landscape change. The historical landscape genetic framework employed in this study is broadly applicable to other agricultural pests and might reveal general responses of pests to agricultural land‐use change.

 
more » « less
NSF-PAR ID:
10460006
Author(s) / Creator(s):
 ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Evolutionary Applications
Volume:
12
Issue:
4
ISSN:
1752-4571
Format(s):
Medium: X Size: p. 804-814
Size(s):
["p. 804-814"]
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Landscape structure, which can be manipulated in agricultural landscapes through crop rotation and modification of field edge habitats, can have important effects on connectivity among local populations of insects. Though crop rotation is known to influence the abundance of Colorado potato beetle (CPB;Leptinotarsa decemlineataSay) in potato (Solanum tuberosumL.) fields each year, whether crop rotation and intervening edge habitat also affect genetic variation among populations is unknown. We investigated the role of landscape configuration and composition in shaping patterns of genetic variation in CPB populations in the Columbia Basin of Oregon and Washington, and the Central Sands of Wisconsin, USA. We compared landscape structure and its potential suitability for dispersal, tested for effects of specific land cover types on genetic differentiation among CPB populations, and examined the relationship between crop rotation distances and genetic diversity. We found higher genetic differentiation between populations separated by low potato land cover, and lower genetic diversity in populations occupying areas with greater crop rotation distances. Importantly, these relationships were only observed in the Columbia Basin, and no other land cover types influenced CPB genetic variation. The lack of signal in Wisconsin may arise as a consequence of greater effective population size and less pronounced genetic drift. Our results suggest that the degree to which host plant land cover connectivity affects CPB genetic variation depends on population size and that power to detect landscape effects on genetic differentiation might be reduced in agricultural insect pest systems.

     
    more » « less
  2. Abstract

    Despite extensive research on agricultural pests, our knowledge about their evolutionary history is often limited. A mechanistic understanding of the demographic changes and modes of adaptation remains an important goal, as it improves our understanding of organismal responses to environmental change and our ability to sustainably manage pest populations. Emerging genomic datasets now allow for characterization of demographic and adaptive processes, but face limits when they are drawn from contemporary samples, especially in the context of strong demographic change, repeated selection, or adaptation involving modest shifts in allele frequency at many loci. Temporal sampling, however, can improve our ability to reconstruct evolutionary events. Here, we leverage museum samples to examine whether population genomic diversity and structure has changed over time, and to identify genomic regions that appear to be under selection. We focus on the Colorado potato beetle (CPB), Leptinotarsa decemlineata (Say 1824; Coleoptera: Chrysomelidae), which is widely regarded as a super-pest due to its rapid, and repeated, evolution to insecticides. By combining whole genome resequencing data from 78 museum samples with modern sampling, we demonstrate that CPB expanded rapidly in the 19th century, leading to a reduction in diversity and limited genetic structure from the Midwest to Northeast United States. Temporal genome scans provide extensive evidence for selection acting in resistant field populations in Wisconsin and New York, including numerous known insecticide resistance genes. We also validate these results by showing that known selective sweeps in modern populations are identified by our genome scan. Perhaps most importantly, temporal analysis indicates selection on standing genetic variation, as we find evidence for parallel evolution in the two geographical regions. Parallel evolution involves a range of phenotypic traits not previously identified as under selection in CPB, such as reproductive and morphological functional pathways that might be important for adaptation to agricultural habitats.

     
    more » « less
  3. Abstract

    Assessing the environmental factors that influence the ability of a threatened species to move through a landscape can be used to identify conservation actions that connect isolated populations. However, direct observations of species' movement are often limited, making the development of alternate approaches necessary. Here we use landscape genetic analyses to assess the impact of landscape features on the movement of individuals between local populations of a threatened snake, the eastern massasauga rattlesnake (Sistrurus catenatus). We linked connectivity data with habitat information from two landscapes of similar size: a large region of unfragmented habitat and a previously studied fragmented landscape consisting of isolated patches of habitat. We used this analysis to identify features of the landscape where modification or acquisition would enhance population connectivity in the fragmented region. We found evidence that current connectivity was impacted by both contemporary land‐cover features, especially roads, and inherent landscape features such as elevation. Next, we derived estimates of expected movement ability using a recently developed pedigree‐based approach and least‐cost paths through the unfragmented landscape. We then used our pedigree and resistance map to estimate resistance polygons of the potential extent forS. catenatusmovement in the fragmented landscape. These polygons identify possible sites for future corridors connecting currently isolated populations in this landscape by linking the impact of future habitat modification or land acquisition to dispersal ability in this species. Overall, our study shows how modeling landscape resistance across differently fragmented landscapes can identify habitat features that affect contemporary movement in threatened species in fragmented landscapes and how this information can be used to guide mitigation actions whose goal is to connect isolated populations.

     
    more » « less
  4. Abstract

    In the context of global decline in old‐growth forest, historical ecology is a valuable tool to derive insights into vegetation legacies and dynamics and develop new conservation and restoration strategies. In this cross‐disciplinary study, we integrate palynology (Lago del Pesce record), history, dendrochronology, and historical and contemporary land cover maps to assess drivers of vegetation change over the last millennium in a Mediterranean mountain forest (Pollino National Park, southern Italy) and discuss implications in conservation ecology. The study site hosts a remnant beech–fir (Fagus sylvaticaAbies alba) mixed forest, a priority habitat for biodiversity conservation in Europe. In the 10th century, the pollen record showed an open environment that was quickly colonized by silver fir when sociopolitical instabilities reduced anthropogenic pressures in mountain forests. The highest forest cover and biomass was reached between the 14th and the 17th centuries following land abandonment due to recurring plague pandemics. This rewilding process is also reflected in the recruitment history of Bosnian pine (Pinus heldreichii) in the subalpine elevation belt. Our results show that human impacts have been one of the main drivers of silver fir population contraction in the last centuries in the Mediterranean, and that the removal of direct human pressure led to ecosystem renovation. Since 1910, the Rubbio State Forest has locally protected and restored the mixed beech–fir forest. The institutions in 1972 for the Rubbio Natural Reserve and in 1993 for Pollino National Park have guaranteed the survival of the silver fir population, demonstrating the effectiveness of targeted conservation and restoration policies despite a warming climate. Monitoring silver fir populations can measure the effectiveness of conservation measures. In the last decades, the abandonment of rural environments (rewilding) along the mountains of southern Italy has reduced the pressure on ecosystems, thus boosting forest expansion. However, after four decades of natural regeneration and increasing biomass, pollen influx and forest composition are still far from the natural attributes of the medieval forest ecosystem. We conclude that long‐term forest planning encouraging limited direct human disturbance will lead toward rewilding and renovation of carbon‐rich and highly biodiverse Mediterranean old‐growth forests, which will be more resistant and resilient to future climate change.

     
    more » « less
  5. Abstract

    Habitat augmentation on farms is predicted to conserve biological diversity and support beneficial animals that reduce crop pests. Effectiveness of local habitat enhancement and subsequent pest reduction services can be mediated by the amount of habitat at larger scales. We tested whether the presence and increase of local and landscape scale bird habitat increased avian predator abundance and pest reduction by birds. We surveyed birds and performed a sentinel prey exclosure experiment in walnut orchards in the Sacramento Valley, California,USA—comparing predation probability between orchards with (n = 10) and without (n = 10) woody habitat in uncultivated orchard margins. We digitized seminatural habitat cover in landscapes around orchards to test the effectiveness of avian predators in reducing sentinel prey along a seminatural cover gradient of 0–38%. Experimental prey were diapausing larvae ofCydia pomonella(L.) (Lepidoptera: Tortricidae; codling moth), a significant pest of walnuts, which overwinter in cocoons in orchards, emerge as adults, and produce larvae that feed on the nuts the following spring. Permitting bird access to cocoons increased larval predation from 11% (caged) to 46% (no cage), and predation increased with increasing proportions of seminatural habitat within 500‐m of orchard transects. Predation also increased as the size and bark furrow depth of walnut trees increased, likely because these characteristics were associated with increasing abundance of avian predators with functional traits specific to consuming tree‐dwelling cocoons (e.g., woodpeckers). The presence and increasing complexity of local margin habitat increased the species richness and abundance of avian predators but was not predictive of cocoon predation. Consistent with intermediate landscape‐complexity hypothesis predictions, the effect size of woodpecker abundance on predation was large in simple landscapes (1–20% seminatural cover) and low in complex landscapes (>20% cover). Contrary to predictions, effect size was large in cleared landscapes (<1% cover), suggesting that orchards supported predators in cleared landscapes, with positive effects on pest reduction. We provide evidence that increasing the abundance of avian predators with traits specific for consuming target pests—by retaining old trees and seminatural cover—can increase orchard pest reduction services in an intensive agricultural region.

     
    more » « less