- Email: [email protected]
The Evolution of Paleoecology
TREE 2636 No. of Pages 3
Trends in Ecology & Evolution
Forum
The Evolution of Paleoecology Joseph D. Napier , 1,*,@ Guillaume de Lafontaine,2 and Melissa L. Chipman3,@
While the interplay between migration and adaptation dictates species response to climate change, technological limitations have obfuscated explicit tests on past adaptive responses. However, a surge in technology-driven advances in paleoecological methods coincides with breakthroughs in processing ancient DNA, providing the first opportunity to assess adaptation to past climate shifts. The Quaternary Conundrum Understanding the response of species to shifting climatic regimes to assess the impacts of ongoing and future climate change is a fundamental theme in both ecology and evolution. Past demographic dynamics have primarily been inferred by integrating paleoecological reconstructions of community composition, surveys of modern genetic diversity, and spatially explicit modeling of past species distributions and climate suitability [1]. As these results accumulate, there remains a stark contrast between the paucity of evidence for past extinctions and the numerous future extinction events predicted by ongoing empirical and theoretical work. This paradox, known as the ‘Quaternary conundrum’, was partly attributed to the unappreciated role of the easily overlooked, isolated microrefugial populations outside predicted climate envelopes [1]. Of potentially greater importance is the cryptic interplay of migration and adaptation in mediating species response to past climate shifts in the Quaternary and beyond. Although recent syntheses have explored
this hypothesis [1,2], technological limitations have largely prevented major advances in explicitly testing the role of adaptation to past climate change.
Paleoecology Meets Ancient DNA: Elucidating Past Adaptation Attempts to understand past adaptive responses to climate shifts were limited by a lack of DNA from subfossil material, corresponding phenotypic information, and high-resolution paleoclimate reconstructions. The application of ancient DNA (aDNA) to resolve past evolutionary and ecological dynamics is a recent paradigm shift, and the reliance on indirect inferences drawn from modern DNA can now be improved by direct observations obtained by analyzing aDNA from historical and ancient remains [3]. Although this cutting-edge technique has led to revolutionary interpretations in the field of human evolution, novel applications of aDNA to studies of paleoecological processes are only beginning to emerge. The proliferation of plant and genome-wide aDNA techniques [4,5] is fortuitously timed with rapid advances in paleo techniques that can provide high-resolution reconstructions of past climate and phenotypes. Some of the most promising new paleoecological analyses include: (i) using pollen morphology to examine past changes in UV irradiance [6]; (ii) phenotypic and paleoclimate information from leaf morphology and leaf-wax isotopes [7,8]; and (iii) scanning electron microscopy (SEM) and computer-learning applications for high-resolution microfossil
imaging [9]. These proxies allow new insights into broad-scale environmental stressors and associated plant phenotypic responses. For example, combining measures of leaf morphology and structures (e.g., stomata and phytoliths) with paleoclimate information from cuticular waxes on the same subfossil material can help identify past ecological strategies in response to drought tolerance. Detecting microscale variations in pollen morphology by training machine-learning algorithms on SEM images can help assess important morphological traits that might be linked to pivotal demographic events such as postglacial expansion. In addition to these advanced paleobased techniques, community-driven efforts to compile existing high-quality paleorecords in accessible databases, such as Neotoma (www.neotomadb.org) and the European Pollen Database (www. europeanpollendatabase.net), has rapidly expanded opportunities to link fine-scale phenotypic information from the fossil record to large-scale climate changes. In addition, a new freeware tool called PaleoView now allows the generation of spatially gridded time series of regional and global climate data for any period over the past 21 000 years [10]. By combining data generated from these emergent paleoecological methods with aDNA, we can leverage established modern frameworks that explore the relationship between genetic variation and phenotypic traits and/or climate (Box 1). Using these frameworks to associate aDNA with past climate and phenotypic
Box 1. Existing Frameworks to Associate Genetic Variation with Climate and Phenotypes. Over the past few decades, several approaches have been developed to assimilate genetic, climatic, and phenotypic data to uncover putative signals of natural selection. The most relevant of these approaches to the integration of aDNA and paleodata are genome‐wide association studies (GWAS) and environmental association analysis (often referred to as genotype environment associations or GEA). GWAS is used to identify genomic regions that are linked to specific phenotypes, while GEA is a tool to correlate environmental data and genotypes [11]. For both methodologies, the goal is to link changes in allele frequencies with shifts in important climate or phenotypic variables. Thus, these analyses provide insight into the potential role of adaptation to different climatic regimes and stressors while also identifying candidate genomic regions that might be involved in a stress response pathway for post hoc validation studies. The implementation of GWAS and GEA for aDNA and paleobotanical evidence will provide the essential first step needed to examine the role of adaptation during periods of past climate shifts.
Trends in Ecology & Evolution, Month 2019, Vol. xx, No. xx
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Trends in Ecology & Evolution
variation, we can elucidate past signals of adaptation, providing novel insight into how species responded to climate change in the geologic past (Figure 1). Genotype-environment associations (GEA) and genome-wide association studies (GWAS) provide evidence of key relationships between genetic variation and current climate conditions as well as observed phenotypes [11]. These associations can lead to the identification of candidate genes or genomic regions responsible for mediating responses to abiotic and biotic stress [11]. Applying these same methods to fossil material, PaleoGEA and PaleoGWAS could identify genomic regions that are important or adaptive during target historical periods of interest. By isolating fossil material, identifying phenotypic characteristics, and applying aDNA techniques, one could link genetic and phenotypic data for any time in the past where material is available, examine those data in the context of temporally relevant climate reconstructions across the landscape, and isolate signatures of adaptation in response to natural selective pressure. While such techniques seemed outside the realm of possibility just a short time ago, a simple study design could be used to collect the necessary data for PaleoGEA and PaleoGWAS. Studies targeting aDNA in plants have been challenging due to complications associated with isolating, extracting, and processing DNA from ancient plant samples, but recent advances and targeted system selection has seen a proliferation in plant aDNA studies from lake sediments Trends in Ecology & Evolution [3]. For example, Quaternary glaciations Figure 1. Integrative Approach to Elucidate Signals of Local Adaptation to (A) Modern-Day and (B) Past Environments. (A) Modern climate data are available from weather stations; phenotypes are obtained have left abundant lakes and wetlands from direct field measurements or laboratory analyses; and whole-genome genotyping can be performed on the landscape that serve as primary after DNA extraction from fresh tissues. Using these datasets, genome-wide association studies (GWAS) target systems for paleoecological studies. and genotype environment associations (GEA) are now commonly used to identify genomic regions Selecting and sampling lake sites across associated with specific phenotypes and modern-day environments, respectively, providing insights into the potential role of adaptation to climate change. (B). Emerging paleoecological techniques can now this vast and heterogeneous landscape generate well-resolved paleophenotypic data, which coincides with the recent availability of associated would provide access to abundant arhigh-resolution paleoclimate reconstructions. These rapid advances in paleodata complement recent chives of pollen and other subfossil material ancient DNA (aDNA) breakthroughs, which provide genetic data from across the entire ancient genome, (e.g., mosses, needles, leaves, seeds, and and open the door for next-generation retrospective studies. Integrating these novel lines of paleoevidence provides the same three elements needed to understand signals of local adaptation on the modern phytoliths), as well as aDNA needed to utilandscape. Implementing paleoGWAS and paleoGEA provides the essential first step in examining the role lize GWAS and GEA in a paleo context. of adaptation during periods of past climate shifts. Targeting depositional systems with the 2
Trends in Ecology & Evolution, Month 2019, Vol. xx, No. xx
Trends in Ecology & Evolution
potential for robust chronologies, such as lakes with abundant macrofossil remains for AMS 14C dating, glacial lakes with varved sediments, and/or basins in regions that have dateable ashfall and tephra deposits would be ideal. A network of sites that captures the full climate gradient within a species range could allow robust interpretations of adaptive responses during demographic processes such as migration, contraction, and expansion.
The Future of Studying the Past The implementation of PaleoGEA and PaleoGWAS will improve our understanding of ecological and evolutionary responses to anthropogenic climate change. For example, while the importance of conditional neutrality is well established in the context of a spatially variable environments, it remains uncertain what gene sets are used to respond to past episodes of climate change [1]. Are some alleles adaptive in the past but neutral in the present? What stress-response genes are under selection during different episodes of climate change? This idea of temporal conditional neutrality could eventually help refine sets of general stress response genes while understanding what set of climatic stressors induce differential selection in contrasting genomic regions. Moreover, if periods of similar climate conditions show that the same genomic regions were under selection, then it may help refine the genomic regions associated with a given stressor without making statistically based judgment calls on which regions are actually important.
Findings from these studies could be combined with ongoing efforts to explicitly integrate disparate lines of modeling, fossil, and genetic evidence [12] to give unparalleled insight into how species survive, migrate, and adapt to a changing world. Furthermore, availability of genetic data from current and past populations will allow for the testing and validation of population genetic models, such as forward demographic models and backward coalescent simulations, by comparing model output with the paleogenetic data. Such paleovalidated population genetic models could then be used to make projections about the genetic diversity of target species under future climate change scenarios. Given lingering uncertainty about the future of many taxa in the face of anthropogenic climate shifts, these timely lessons will help constrain future estimates of loss and better project the impact of ongoing climate change. Ultimately, recent improvements in collecting and sequencing genomewide aDNA coincides with a surge in technology-driven advances in paleoecological data analyses, and the potential collaborative opportunity between these data sources has set the stage for unprecedented advances in the way we study the past.
*Correspondence: [email protected] (J.D. Napier). @ Twitter: @J_D_Napier (J. Napier) and @mchipman5 (M. Chipman). https://doi.org/10.1016/j.tree.2019.12.006 © 2019 Elsevier Ltd. All rights reserved.
References 1. de Lafontaine, G. et al. (2018) Invoking adaptation to decipher the genetic legacy of past climate change. Ecology 99, 1530–1546 2. Nogués-Bravo, D. et al. (2018) Cracking the code of biodiversity responses to past climate change. Trends Ecol. Evol. 33, 765–776 3. Parducci, L. et al. (2017) Ancient plant DNA in lake sediments. New Phytol. 214, 924–942 4. Estrada, O. et al. (2018) Ancient plant DNA in the genomic era. Nat. Plants 4, 394 5. Wagner, S. et al. (2018) High-Throughput DNA sequencing of ancient wood. Mol. Ecol. 27, 1138–1154 6. Seddon, A.W. et al. (2019) Fossil pollen and spores as a tool for reconstructing ancient solar-ultraviolet irradiance received by plants: an assessment of prospects and challenges using proxy-system modelling. Photochem. Photobiol. Sci. 18, 275–294 7. Benítez, J.J. et al. (2019) Applications and potentialities of atomic force microscopy in fossil and extant plant cuticle characterization. Rev. Palaeobot. Palynol. 268, 125–132 8. Daniels, W.C. et al. (2018) Effect of continuous light on leaf wax isotope ratios in Betula nana and Eriophorum vaginatum: implications for Arctic paleoclimate reconstructions. Org. Geochem. 125, 70–81 9. Mander, L. and Punyasena, S.W. (2018) Fossil pollen and spores in paleoecology. In Methods in Paleoecology (Croft, D.A. et al., eds), pp. 215–234, Springer 10. Fordham, D.A. et al. (2017) PaleoView: a tool for generating continuous climate projections spanning the last 21 000 years at regional and global scales. Ecography 40, 1348–1358 11. Rellstab, C. et al. (2015) A practical guide to environmental association analysis in landscape genomics. Mol. Ecol. 24, 4348–4370 12. Hoban, S. et al. (2019) Inference of biogeographic history by formally integrating distinct lines of evidence: genetic, environmental niche and fossil. Ecography 42, 1991–2011
1
Department of Integrative Biology, The University of Texas at Austin, Austin, TX 78712, USA 2 Canada Research Chair in Integrative Biology of Northern Flora, Université du Québec à Rimouski, Rimouski, QC G5L 3A1, Canada 3 Department of Earth Sciences, Syracuse University, Syracuse, NY 13244, USA
Trends in Ecology & Evolution, Month 2019, Vol. xx, No. xx
3
Trends in Ecology & Evolution
Forum
The Evolution of Paleoecology Joseph D. Napier , 1,*,@ Guillaume de Lafontaine,2 and Melissa L. Chipman3,@
While the interplay between migration and adaptation dictates species response to climate change, technological limitations have obfuscated explicit tests on past adaptive responses. However, a surge in technology-driven advances in paleoecological methods coincides with breakthroughs in processing ancient DNA, providing the first opportunity to assess adaptation to past climate shifts. The Quaternary Conundrum Understanding the response of species to shifting climatic regimes to assess the impacts of ongoing and future climate change is a fundamental theme in both ecology and evolution. Past demographic dynamics have primarily been inferred by integrating paleoecological reconstructions of community composition, surveys of modern genetic diversity, and spatially explicit modeling of past species distributions and climate suitability [1]. As these results accumulate, there remains a stark contrast between the paucity of evidence for past extinctions and the numerous future extinction events predicted by ongoing empirical and theoretical work. This paradox, known as the ‘Quaternary conundrum’, was partly attributed to the unappreciated role of the easily overlooked, isolated microrefugial populations outside predicted climate envelopes [1]. Of potentially greater importance is the cryptic interplay of migration and adaptation in mediating species response to past climate shifts in the Quaternary and beyond. Although recent syntheses have explored
this hypothesis [1,2], technological limitations have largely prevented major advances in explicitly testing the role of adaptation to past climate change.
Paleoecology Meets Ancient DNA: Elucidating Past Adaptation Attempts to understand past adaptive responses to climate shifts were limited by a lack of DNA from subfossil material, corresponding phenotypic information, and high-resolution paleoclimate reconstructions. The application of ancient DNA (aDNA) to resolve past evolutionary and ecological dynamics is a recent paradigm shift, and the reliance on indirect inferences drawn from modern DNA can now be improved by direct observations obtained by analyzing aDNA from historical and ancient remains [3]. Although this cutting-edge technique has led to revolutionary interpretations in the field of human evolution, novel applications of aDNA to studies of paleoecological processes are only beginning to emerge. The proliferation of plant and genome-wide aDNA techniques [4,5] is fortuitously timed with rapid advances in paleo techniques that can provide high-resolution reconstructions of past climate and phenotypes. Some of the most promising new paleoecological analyses include: (i) using pollen morphology to examine past changes in UV irradiance [6]; (ii) phenotypic and paleoclimate information from leaf morphology and leaf-wax isotopes [7,8]; and (iii) scanning electron microscopy (SEM) and computer-learning applications for high-resolution microfossil
imaging [9]. These proxies allow new insights into broad-scale environmental stressors and associated plant phenotypic responses. For example, combining measures of leaf morphology and structures (e.g., stomata and phytoliths) with paleoclimate information from cuticular waxes on the same subfossil material can help identify past ecological strategies in response to drought tolerance. Detecting microscale variations in pollen morphology by training machine-learning algorithms on SEM images can help assess important morphological traits that might be linked to pivotal demographic events such as postglacial expansion. In addition to these advanced paleobased techniques, community-driven efforts to compile existing high-quality paleorecords in accessible databases, such as Neotoma (www.neotomadb.org) and the European Pollen Database (www. europeanpollendatabase.net), has rapidly expanded opportunities to link fine-scale phenotypic information from the fossil record to large-scale climate changes. In addition, a new freeware tool called PaleoView now allows the generation of spatially gridded time series of regional and global climate data for any period over the past 21 000 years [10]. By combining data generated from these emergent paleoecological methods with aDNA, we can leverage established modern frameworks that explore the relationship between genetic variation and phenotypic traits and/or climate (Box 1). Using these frameworks to associate aDNA with past climate and phenotypic
Box 1. Existing Frameworks to Associate Genetic Variation with Climate and Phenotypes. Over the past few decades, several approaches have been developed to assimilate genetic, climatic, and phenotypic data to uncover putative signals of natural selection. The most relevant of these approaches to the integration of aDNA and paleodata are genome‐wide association studies (GWAS) and environmental association analysis (often referred to as genotype environment associations or GEA). GWAS is used to identify genomic regions that are linked to specific phenotypes, while GEA is a tool to correlate environmental data and genotypes [11]. For both methodologies, the goal is to link changes in allele frequencies with shifts in important climate or phenotypic variables. Thus, these analyses provide insight into the potential role of adaptation to different climatic regimes and stressors while also identifying candidate genomic regions that might be involved in a stress response pathway for post hoc validation studies. The implementation of GWAS and GEA for aDNA and paleobotanical evidence will provide the essential first step needed to examine the role of adaptation during periods of past climate shifts.
Trends in Ecology & Evolution, Month 2019, Vol. xx, No. xx
1
Trends in Ecology & Evolution
variation, we can elucidate past signals of adaptation, providing novel insight into how species responded to climate change in the geologic past (Figure 1). Genotype-environment associations (GEA) and genome-wide association studies (GWAS) provide evidence of key relationships between genetic variation and current climate conditions as well as observed phenotypes [11]. These associations can lead to the identification of candidate genes or genomic regions responsible for mediating responses to abiotic and biotic stress [11]. Applying these same methods to fossil material, PaleoGEA and PaleoGWAS could identify genomic regions that are important or adaptive during target historical periods of interest. By isolating fossil material, identifying phenotypic characteristics, and applying aDNA techniques, one could link genetic and phenotypic data for any time in the past where material is available, examine those data in the context of temporally relevant climate reconstructions across the landscape, and isolate signatures of adaptation in response to natural selective pressure. While such techniques seemed outside the realm of possibility just a short time ago, a simple study design could be used to collect the necessary data for PaleoGEA and PaleoGWAS. Studies targeting aDNA in plants have been challenging due to complications associated with isolating, extracting, and processing DNA from ancient plant samples, but recent advances and targeted system selection has seen a proliferation in plant aDNA studies from lake sediments Trends in Ecology & Evolution [3]. For example, Quaternary glaciations Figure 1. Integrative Approach to Elucidate Signals of Local Adaptation to (A) Modern-Day and (B) Past Environments. (A) Modern climate data are available from weather stations; phenotypes are obtained have left abundant lakes and wetlands from direct field measurements or laboratory analyses; and whole-genome genotyping can be performed on the landscape that serve as primary after DNA extraction from fresh tissues. Using these datasets, genome-wide association studies (GWAS) target systems for paleoecological studies. and genotype environment associations (GEA) are now commonly used to identify genomic regions Selecting and sampling lake sites across associated with specific phenotypes and modern-day environments, respectively, providing insights into the potential role of adaptation to climate change. (B). Emerging paleoecological techniques can now this vast and heterogeneous landscape generate well-resolved paleophenotypic data, which coincides with the recent availability of associated would provide access to abundant arhigh-resolution paleoclimate reconstructions. These rapid advances in paleodata complement recent chives of pollen and other subfossil material ancient DNA (aDNA) breakthroughs, which provide genetic data from across the entire ancient genome, (e.g., mosses, needles, leaves, seeds, and and open the door for next-generation retrospective studies. Integrating these novel lines of paleoevidence provides the same three elements needed to understand signals of local adaptation on the modern phytoliths), as well as aDNA needed to utilandscape. Implementing paleoGWAS and paleoGEA provides the essential first step in examining the role lize GWAS and GEA in a paleo context. of adaptation during periods of past climate shifts. Targeting depositional systems with the 2
Trends in Ecology & Evolution, Month 2019, Vol. xx, No. xx
Trends in Ecology & Evolution
potential for robust chronologies, such as lakes with abundant macrofossil remains for AMS 14C dating, glacial lakes with varved sediments, and/or basins in regions that have dateable ashfall and tephra deposits would be ideal. A network of sites that captures the full climate gradient within a species range could allow robust interpretations of adaptive responses during demographic processes such as migration, contraction, and expansion.
The Future of Studying the Past The implementation of PaleoGEA and PaleoGWAS will improve our understanding of ecological and evolutionary responses to anthropogenic climate change. For example, while the importance of conditional neutrality is well established in the context of a spatially variable environments, it remains uncertain what gene sets are used to respond to past episodes of climate change [1]. Are some alleles adaptive in the past but neutral in the present? What stress-response genes are under selection during different episodes of climate change? This idea of temporal conditional neutrality could eventually help refine sets of general stress response genes while understanding what set of climatic stressors induce differential selection in contrasting genomic regions. Moreover, if periods of similar climate conditions show that the same genomic regions were under selection, then it may help refine the genomic regions associated with a given stressor without making statistically based judgment calls on which regions are actually important.
Findings from these studies could be combined with ongoing efforts to explicitly integrate disparate lines of modeling, fossil, and genetic evidence [12] to give unparalleled insight into how species survive, migrate, and adapt to a changing world. Furthermore, availability of genetic data from current and past populations will allow for the testing and validation of population genetic models, such as forward demographic models and backward coalescent simulations, by comparing model output with the paleogenetic data. Such paleovalidated population genetic models could then be used to make projections about the genetic diversity of target species under future climate change scenarios. Given lingering uncertainty about the future of many taxa in the face of anthropogenic climate shifts, these timely lessons will help constrain future estimates of loss and better project the impact of ongoing climate change. Ultimately, recent improvements in collecting and sequencing genomewide aDNA coincides with a surge in technology-driven advances in paleoecological data analyses, and the potential collaborative opportunity between these data sources has set the stage for unprecedented advances in the way we study the past.
*Correspondence: [email protected] (J.D. Napier). @ Twitter: @J_D_Napier (J. Napier) and @mchipman5 (M. Chipman). https://doi.org/10.1016/j.tree.2019.12.006 © 2019 Elsevier Ltd. All rights reserved.
References 1. de Lafontaine, G. et al. (2018) Invoking adaptation to decipher the genetic legacy of past climate change. Ecology 99, 1530–1546 2. Nogués-Bravo, D. et al. (2018) Cracking the code of biodiversity responses to past climate change. Trends Ecol. Evol. 33, 765–776 3. Parducci, L. et al. (2017) Ancient plant DNA in lake sediments. New Phytol. 214, 924–942 4. Estrada, O. et al. (2018) Ancient plant DNA in the genomic era. Nat. Plants 4, 394 5. Wagner, S. et al. (2018) High-Throughput DNA sequencing of ancient wood. Mol. Ecol. 27, 1138–1154 6. Seddon, A.W. et al. (2019) Fossil pollen and spores as a tool for reconstructing ancient solar-ultraviolet irradiance received by plants: an assessment of prospects and challenges using proxy-system modelling. Photochem. Photobiol. Sci. 18, 275–294 7. Benítez, J.J. et al. (2019) Applications and potentialities of atomic force microscopy in fossil and extant plant cuticle characterization. Rev. Palaeobot. Palynol. 268, 125–132 8. Daniels, W.C. et al. (2018) Effect of continuous light on leaf wax isotope ratios in Betula nana and Eriophorum vaginatum: implications for Arctic paleoclimate reconstructions. Org. Geochem. 125, 70–81 9. Mander, L. and Punyasena, S.W. (2018) Fossil pollen and spores in paleoecology. In Methods in Paleoecology (Croft, D.A. et al., eds), pp. 215–234, Springer 10. Fordham, D.A. et al. (2017) PaleoView: a tool for generating continuous climate projections spanning the last 21 000 years at regional and global scales. Ecography 40, 1348–1358 11. Rellstab, C. et al. (2015) A practical guide to environmental association analysis in landscape genomics. Mol. Ecol. 24, 4348–4370 12. Hoban, S. et al. (2019) Inference of biogeographic history by formally integrating distinct lines of evidence: genetic, environmental niche and fossil. Ecography 42, 1991–2011
1
Department of Integrative Biology, The University of Texas at Austin, Austin, TX 78712, USA 2 Canada Research Chair in Integrative Biology of Northern Flora, Université du Québec à Rimouski, Rimouski, QC G5L 3A1, Canada 3 Department of Earth Sciences, Syracuse University, Syracuse, NY 13244, USA
Trends in Ecology & Evolution, Month 2019, Vol. xx, No. xx
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