skip to main content


Title: Precipitation and vegetation shape patterns of genomic and craniometric variation in the central African rodent Praomys misonnei
Predicting species' capacity to respond to climate change is an essential first step in developing effective conservation strategies. However, conservation prioritization schemes rarely take evolutionary potential into account. Ecotones provide important opportunities for diversifying selection and may thus constitute reservoirs of standing variation, increasing the capacity for future adaptation. Here, we map patterns of environmentally associated genomic and craniometric variation in the central African rodent Praomys misonnei to identify areas with the greatest turnover in genomic composition. We also project patterns of environmentally associated genomic variation under future climate change scenarios to determine where populations may be under the greatest pressure to adapt. While precipitation gradients influence both genomic and craniometric variation, vegetation structure is also an important determinant of craniometric variation. Areas of elevated environmentally associated genomic and craniometric variation overlap with zones of rapid ecological transition underlining their importance as reservoirs of evolutionary potential. We also find that populations in the Sanaga river basin, central Cameroon and coastal Gabon are likely to be under the greatest pressure from climate change. Lastly, we make specific conservation recommendations on how to protect zones of high evolutionary potential and identify areas where populations may be the most susceptible to climate change.  more » « less
Award ID(s):
1933351
NSF-PAR ID:
10294802
Author(s) / Creator(s):
; ; ; ; ; ; ; ; ; ; ; ; ; ;
Date Published:
Journal Name:
Proceedings of the Royal Society B: Biological Sciences
Volume:
287
Issue:
1930
ISSN:
0962-8452
Page Range / eLocation ID:
20200449
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Preserving biodiversity under rapidly changing climate conditions is challenging. One approach for estimating impacts and their magnitude is to model current relationships between genomic and environmental data and then to forecast those relationships under future climate scenarios. In this way, understanding future genomic and environmental relationships can help guide management decisions, such as where to establish new protected areas where populations might be buffered from high temperatures or major changes in rainfall. However, climate warming is only one of many anthropogenic threats one must consider in rapidly developing parts of the world. In Central Africa, deforestation, mining, and infrastructure development are accelerating population declines of rainforest species. Here we investigate multiple anthropogenic threats in a Central African rainforest songbird, the little greenbul (Andropadus virens). We examine current climate and genomic variation in order to explore the association between genome and environment under future climate conditions. Specifically, we estimateGenomic Vulnerability, defined as the mismatch between current and predicted future genomic variation based on genotype–environment relationships modeled across contemporary populations. We do so while considering other anthropogenic impacts. We find that coastal and central Cameroon populations will require the greatest shifts in adaptive genomic variation, because both climate and land use in these areas are predicted to change dramatically. In contrast, in the more northern forest–savanna ecotones, genomic shifts required to keep pace with climate will be more moderate, and other anthropogenic impacts are expected to be comparatively low in magnitude. While an analysis of diverse taxa will be necessary for making comprehensive conservation decisions, the species‐specific results presented illustrate how evolutionary genomics and other anthropogenic threats may be mapped and used to inform mitigation efforts. To this end, we present an integrated conceptual model demonstrating how the approach for a single species can be expanded to many taxonomically diverse species.

     
    more » « less
  2. Abstract

    Identifying areas of high evolutionary potential is a judicious strategy for developing conservation priorities in the face of environmental change. For wide‐ranging species occupying heterogeneous environments, the evolutionary forces that shape distinct populations can vary spatially. Here, we investigate patterns of genomic variation and genotype–environment associations in the hermit thrush (Catharus guttatus), a North American songbird, at broad (across the breeding range) and narrow spatial scales (at a hybrid zone). We begin by building a genoscape or map of genetic variation across the breeding range and find five distinct genetic clusters within the species, with the greatest variation occurring in the western portion of the range. Genotype–environment association analyses indicate higher allelic turnover in the west than in the east, with measures of temperature surfacing as key predictors of putative adaptive genomic variation rangewide. Since broad patterns detected across a species' range represent the aggregate of many locally adapted populations, we investigate whether our broadscale analysis is consistent with a finer scale analysis. We find that top rangewide temperature‐associated loci vary in their clinal patterns (e.g., steep clines vs. fixed allele frequencies) across a hybrid zone in British Columbia, suggesting that the environmental predictors and the associated candidate loci identified in the rangewide analysis are of variable importance in this particular region. However, two candidate loci exhibit strong concordance with the temperature gradient in British Columbia, suggesting a potential role for temperature‐related barriers to gene flow and/or temperature‐driven ecological selection in maintaining putative local adaptation. This study demonstrates how patterns identified at the broad (macrogeographic) scale can be validated by investigating genotype–environment correlations at the local (microgeographic) scale. Furthermore, our results highlight the importance of considering the spatial distribution of putative adaptive variation when assessing population‐level sensitivity to climate change and other stressors.

     
    more » « less
  3. Abstract

    Historical periods of rapid climate change and associated direct and indirect impacts such as glaciation and restructuring of drainage systems are important in shaping biodiversity, lineage divergence, and contemporary genetic variation amongst many aquatic taxa. Through an understanding of the impacts of these ancient changes in land‐ and waterscapes on current diversity, practitioners can account for a species' unique evolutionary history when developing conservation strategies.

    We investigated intraspecific genetic diversity of the critically endangered freshwater mussel,Lampsilis rafinesqueana, endemic to the interior region of the U.S.A. Our study (1) characterises genetic variation within and amongst populations to infer biogeographic history and (2) applies genetic information to potential conservation strategies. We applied restriction‐site associated DNA sequencing and mitochondrial DNA sequencing to investigate genetic diversity within and amongst populations ofL. rafinesqueanafrom across the species' distribution. We then considered this information in the context of historical riverscape processes and applicability to conservation.

    Variation within rivers was similar, but we found different genetic populations associated with two major ecoregions, the Central Interior Highlands and Osage Plains. The plains population displayed anNevalue approximately 10‐fold lower than the highlands population. Historical demographic modelling suggests the two populations diverged approximately 1.2 million years ago and then both populations underwent a substantial decrease in population size around 19,700 years ago. These two major events are each correlated with known periods of historic rapid climate change.

    We identified two distinct populations of a federally endangered mussel,L. rafinesqueana. Contemporary genetic diversity of this species was strongly influenced by direct and indirect impacts of rapid historic shifts in climate. The highlands population has undergone a recent expansion, typical of post‐Pleistocene climate change, while also having a much largerNevalue than the plains population. Our results suggest low levels of gene flow amongst the two distinct populations across generations. We recommend that conservation managers for this species take into account relative difference in diversity between populations when developing management strategies. In many species, assisted gene flow amongst genetically unique populations should only be considered in extreme circumstances; however, inL. rafinesqueana, low levels of assisted migration amongst populations may be a valuable tactic to maintain natural levels of genetic variation.

    Our study shows that biogeographical frameworks can be useful for developing conservation strategies that serve to retain important genomic variation that represents the evolutionary potential of target freshwater species.

     
    more » « less
  4. Abstract

    As climate change advances, environmental gradients may decouple, generating novel multivariate environments that stress wild populations. A commonly invoked mechanism of evolutionary rescue is adaptive gene flow tracking climate shifts, but gene flow from populations inhabiting similar conditions on one environmental axis could cause maladaptive introgression when populations are adapted to different environmental variables that do not shift together. Genomic architecture can play an important role in determining the effectiveness and relative magnitudes of adaptive gene flow and in situ adaptation. This may have direct consequences for how species respond to climate change but is often overlooked. Here, we simulated microevolutionary responses to environmental change under scenarios defined by variation in the polygenicity, linkage, and genetic redundancy of two independent traits, one of which is adapted to a gradient that shifts under climate change. We used these simulations to examine how genomic architecture influences evolutionary outcomes under climate change. We found that climate‐tracking (up‐gradient) gene flow, though present in all scenarios, was strongly constrained under scenarios of lower linkage and higher polygenicity and redundancy, suggesting in situ adaptation as the predominant mechanism of evolutionary rescue under these conditions. We also found that high polygenicity caused increased maladaptation and demographic decline, a concerning result given that many climate‐adapted traits may be polygenic. Finally, in scenarios with high redundancy, we observed increased adaptive capacity. This finding adds to the growing recognition of the importance of redundancy in mediating in situ adaptive capacity and suggests opportunities for better understanding the climatic vulnerability of real populations.

     
    more » « less
  5. Abstract

    Identifying genetic conservation units (CUs) in threatened species is critical for the preservation of adaptive capacity and evolutionary potential in the face of climate change. However, delineating CUs in highly mobile species remains a challenge due to high rates of gene flow and genetic signatures of isolation by distance. Even when CUs are delineated in highly mobile species, the CUs often lack key biological information about what populations have the most conservation need to guide management decisions. Here we implement a framework for CU identification in the Canada Warbler (Cardellina canadensis), a migratory bird species of conservation concern, and then integrate demographic modelling and genomic offset to guide conservation decisions. We find that patterns of whole genome genetic variation in this highly mobile species are primarily driven by putative adaptive variation. Identification of CUs across the breeding range revealed that Canada Warblers fall into two evolutionarily significant units (ESU), and three putative adaptive units (AUs) in the South, East, and Northwest. Quantification of genomic offset, a metric of genetic changes necessary to maintain current gene–environment relationships, revealed significant spatial variation in climate vulnerability, with the Northwestern AU being identified as the most vulnerable to future climate change. Alternatively, quantification of past population trends within each AU revealed the steepest population declines have occurred within the Eastern AU. Overall, we illustrate that genomics‐informed CUs provide a strong foundation for identifying current and future regional threats that can be used to inform management strategies for a highly mobile species in a rapidly changing world.

     
    more » « less