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Recentering evolution for sustainability science

Published online by Cambridge University Press:  05 February 2024

Ella Vázquez-Domínguez*
Affiliation:
Departamento de Ecología de la Biodiversidad, Instituto de Ecología, Universidad Nacional Autónoma de México, Ciudad Universitaria, CP 04510 Ciudad de México, Mexico
Rees Kassen
Affiliation:
Department of Biology, McGill University, Montreal, QC, Canada
Sibylle Schroer
Affiliation:
Leibniz Institute of Freshwater Ecology and Inland Fisheries (IGB), Berlin, Germany
Luc De Meester
Affiliation:
Leibniz Institute of Freshwater Ecology and Inland Fisheries (IGB), Berlin, Germany Laboratory of Aquatic Ecology, Evolution and Conservation, KU Leuven, Leuven, Belgium Institute of Biology, Freie Universität Berlin, Berlin, Germany
Marc T. J. Johnson
Affiliation:
Department of Biology & Centre for Urban Environments, University of Toronto Mississauga, Mississauga, ON, Canada
*
Corresponding author: Ella Vázquez-Domínguez; Email: evazquez@ecologia.unam.mx

Abstract

Non-technical summary

Evolutionary biology considers how organisms and populations change over multiple generations, and so is naturally focused on issues of sustainability through time. Yet, sustainability science rarely incorporates evolutionary thinking and most scientists and policy makers do not account for how evolutionary processes contribute to sustainability. Understanding the interplay between evolutionary processes and nature's contribution to people is key to sustaining life on Earth.

Technical summary

Evolution, the change in gene frequencies within populations, is a process of genetically based modification by descent, providing the raw material essential for adaptation to environmental change. Therefore, it is crucial that we understand evolutionary processes if we aim for a sustainable planet. We here contribute to this development by describing examples of contemporary, rapid evolutionary changes of concern for sustainability, specifically highlighting the global spread of severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) and how the evolutionary toolbox allowed tracking the origins and evolution of SARS-CoV-2 in real time and predicting potential future outbreaks. We also consider how urban development accelerates evolutionary processes such as altered phenotypic and physiological changes and the spread of infectious and zoonotic diseases. We show the importance of evolutionary concepts and techniques for public-health decision making. Many examples of the potential of evolutionary insights contributing to crucial sustainability challenges exist, including infectious and zoonotic diseases, ecosystem and human health, and conservation of natural resources. We thus join recent calls advocating for a stronger collaboration between evolutionary biologists and the sustainability community, increasing interdisciplinarity and the awareness about the knowledge of evolutionary processes for decision making and policies.

Social media summary

Evolution is fundamental to sustaining life on Earth and should be incorporated in sustainability measures and policies.

Type
Intelligence Briefing
Creative Commons
Creative Common License - CCCreative Common License - BY
This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution and reproduction, provided the original article is properly cited.
Copyright
Copyright © The Author(s), 2024. Published by Cambridge University Press

1. Introduction

Evolution is the process of genetically based modification by descent across generations, with genetic variation providing the raw material essential for evolution by natural selection, allowing populations to adapt to environmental change. If genetic diversity is lost, the resilience of ecosystems and their associated services are reduced. Therefore, it is crucial that we understand evolutionary processes if we aim for a sustainable planet (Exposito et al., Reference Exposito-Alonso, Booker, Czech, Gillespie, Hateley, Kyriazis, Lang, Leventhal, Nogues-Bravo, Pagowski, Ruffley, Spence, Toro Arana, Weiß and Zess2022).

Sustainability science studies the interactions between natural and social systems, and how those interactions impact the central goal of sustainability: meeting the needs of present and future generations while substantially increasing human well-being and maintaining the planet's life support systems (Clark & Dickson, Reference Clark and Dickson2003). This emphasis in human and environmental health through time means sustainability science and evolution share a common conceptual lens focused on change across generations. Yet, despite sustainability science being an interdisciplinary subject spanning natural, social, economic, and technological sciences, most scientists and policy makers do not make a direct connection to evolutionary biology (Díaz et al., Reference Díaz, Zafra-Calvo, Purvis, Verburg, Obura, Leadley, Chaplin-Kramer, De Meester, Dulloo, Martín-López, Shaw, Visconti, Broadgate, Bruford, Burgess, Cavender-Bares, DeClerck, Fernández-Palacios, Garibaldi and Zanne2020; Messerli et al., Reference Messerli, Kim, Lutz, Moatti, Richardson, Saidam, Smith, Eloundou-Enyegue, Foli, Glassman, Licona, Murniningtyas, Staniškis, van Ypersele and Furman2019).

We acknowledge the importance of macroevolutionary processes, where evolutionary change driven by selection, gene flow, drift, or mutation can lead to populations with unique combinations of traits and to the origin of new species. But although speciation is often a slow process, trait evolution within populations can be rapid, occurring on contemporary timescales that impact sustainability. Here, we show how evolutionary insights and the evolutionary toolbox – the suite of analytical tools and techniques used to study contemporary evolution – contribute to meeting crucial sustainability challenges. We specifically describe the global spread of severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2), the virus that causes coronavirus disease-2019, as an example that underscores the importance of evolutionary concepts and techniques for public-health decision making. We emphasize how evolutionary tools for comparative genomic analyses and phylogenetic reconstruction provide insight into the genetic changes responsible for the origin and spread of virus variants and play a central role in identifying genetic targets for vaccine development and anti-viral medication. We also underline how urban environments have accelerated contemporary evolutionary processes, often with negative consequences, briefly discussing some examples including the spread of diseases and the evolution of invasive species and impacts on wildlife and human health. We conclude that evolutionary principles, combined with insights from other disciplines including ecology, virology, geography, and economics allow us to address the role of evolution in the provision of ecosystem services and hence, ultimately informing efforts to achieve sustainability measures and policies that are key to sustaining life on Earth.

2. Tracking the origins and evolution of SARS-CoV-2 in real time

SARS-CoV-2, like all RNA viruses, evolves rapidly due to its high mutation rate (spontaneous mutation rate of 1.3 × 10−6; Amicone et al., Reference Amicone, Borges, Alves, Isidro, Zé-Zé, Duarte, Vieira, Guiomar, Gomes and Gordo2022). Rapid genome sequencing of viral isolates shared through public repositories allows tracking the evolution of the virus in near real time (Singh & Yi, Reference Singh and Yi2021), providing insight into emerging variants of concern that can be used to support public-health decision making (see, e.g. https://covarr-net.github.io/duotang/duotang.html#Introduction). The result has been an explosion of genomic data since the first sequence was published in early January 2020, with over 15,389,037 genome sequence submissions now available and more being published every day. These genomic resources have provided unprecedented insight into important aspects of the origins of SARS-CoV-2, such as the key genetic changes thought to allow the virus to cross the species barrier from animals into humans (Andersen et al., Reference Andersen, Rambaut, Lipkin, Holmes and Garry2020).

Phylogenetic analyses, part of the evolutionary toolbox contributing to genomic epidemiology (Grubaugh et al., Reference Grubaugh, Ladner, Lemey, Pybus, Rambaut, Holmes and Andersen2019), reveal the date of the first human infection sometime between late November and mid-December 2019 (Hill & Rambaut, Reference Hill and Rambaut2020; Li et al., Reference Li, Zai, Zhao, Nie, Li, Foley and Chaillon2020). Such methods continue to provide insight into the transmission dynamics and spread of viral strains regionally and globally. Genomic analyses also reveal highly conserved regions where mutations are rare. These can assist in the development of vaccines and antiviral interventions. Ongoing research focuses on specific sites in genome showing evidence of selection that impact transmission or virulence, as well as analytical strategies needed to identify strains bearing these mutations as early as possible (Cyrus et al., Reference Cyrus, Bartha, Weaver, di Iulio, Ferri, Soriaga, Lempp, Hie, Bryson, Berger, Robertson, Snell, Corti, Virgin, Kosakovsky Pond and Telenti2022; Obermeyer et al., Reference Obermeyer, Jankowiak, Barkas, Schaffner, Pyle, Yurkovetskiy, Bosso, Park, Babadi, Macinnis, Luban, Sabeti and Lemieux2022).

The repeated spread of variants of concern – viral genotypes that have a demonstrated impact on human health either because they are more transmissible or more virulent (or both) – is driven by the high mutation rates and extremely large viral population sizes resulting from rapid transmission (Visher et al., Reference Visher, Evensen, Guth, Lai, Norfolk, Rozins, Sokolov, Sui and Boots2021). Competition among genetically distinct viral variants has led to the spread of ever more transmissible forms of the virus, an evolutionary dynamic that closely resembles that seen both in laboratory evolution experiments with microbes (Good et al., Reference Good, McDonald, Barrick, Lenski and Desai2017) and in theoretical models (e.g. Gandon et al., Reference Gandon, Day, Metcalf and Grenfell2016). The role of selection within and among patients in generating variants of concern, especially in the context of a changing immunity landscape for the virus, remains an active area of investigation. Knowing when and where a zoonotic outbreak is likely to occur, namely when a virus whose normal host is an animal species gains the ability to cross the species barrier and causes infection in humans, remains an enormous challenge (Hernandez-Castro et al., Reference Hernandez-Castro, Villacís, Jacobs, Cheaib, Day, Ocaña-Mayorga, Yumiseva, Bacigalupo, Andersson, Matthews, Landguth, Costales, Llewellyn and GrijalvaI2022). Notably, evolutionary tools have enabled analyses of the transmission of SARS-CoV-2 between human and non-human species and to identify mutations associated with each species (Naderi et al., Reference Naderi, Chen, Murall, Poujol, Kraemer, Pickering, Sagan and Shapiro2023), where for instance animal-to-human transmission from minks was detected to be higher compared with lower transmission from other species (cats, dogs, and deer). Hence, continuous molecular surveillance of SARS-CoV-2 from animals is paramount to reveal new insights into SARS-CoV-2 host range and adaptation, contributing to our understanding of the risk of reinfection from animal reservoirs back into humans (Naderi et al., Reference Naderi, Chen, Murall, Poujol, Kraemer, Pickering, Sagan and Shapiro2023).

3. Zoonotic outbreaks and vector dispersal

Not only coronaviruses but a myriad of other viruses, bacteria, parasites, and fungi can cause zoonoses, infectious diseases that are transmitted between species from animals to humans, or from humans to animals, for which forecasting spillover risk and outbreaks is crucial. Zoonotic outbreaks should be unusual because a virus that thrives in one animal species may not possess the mechanism allowing it to establish (i.e. replicate) in a human cell and transmit from person-to-person (Randolph & Rogers, Reference Randolph and Rogers2010). Multiple genetic changes are often required, though we do not typically know a priori how many or which specific environmental conditions promote their evolution (Naderi et al., Reference Naderi, Chen, Murall, Poujol, Kraemer, Pickering, Sagan and Shapiro2023; Visher et al., Reference Visher, Evensen, Guth, Lai, Norfolk, Rozins, Sokolov, Sui and Boots2021). The principles governing the evolution of novelty suggest that any factor which increase the likelihood of a rare mutation contributing to a novel trait, either through genetic mechanisms like gene amplification or ecological ones like increased population size, can enhance the chance that novelty will evolve (Kassen, Reference Kassen2019). While only a small fraction of the thousands of animal viruses with zoonotic potential have led to public health emergencies (Albery et al., Reference Albery, Becker, Brierley, Brook, Christofferson, Cohen, Dallas, Eskew, Fagre, Farrell, Glennon, Guth, Joseph, Mollentze, Neely, Poisot, Rasmussen, Ryan, Seifert and Carlson2021), evidence suggests a growing number of viruses are spilling over into human hosts (Smith et al., Reference Smith, Goldberg, Rosenthal, Carlson, Chen, Chen and Ramachandran2014). The more often spillover happens, the more chances the right combination of mutations allowing infection within and transmission among human hosts will evolve (Visher et al., Reference Visher, Evensen, Guth, Lai, Norfolk, Rozins, Sokolov, Sui and Boots2021), making zoonotic infectious diseases a major sustainability challenge.

Effective tools for forecasting the occurrence and dynamics of outbreaks and the evolution of variants requiring public health attention after an outbreak are being developed (Campbell et al., Reference Campbell, Gifford, Singer, Hill, O'Toole, Rambaut, Hampson and Brunker2022; Polonsky et al., Reference Polonsky, Baidjoe, Kamvar, Cori, Durski, Edmunds, Eggo, Funk, Kaiser, Keating, de Waroux, Marks, Moraga, Morgan, Nouvellet, Ratnayake, Roberts, Whitworth and Jombart2019). A novel approach proposed by Campbell et al. (Reference Campbell, Gifford, Singer, Hill, O'Toole, Rambaut, Hampson and Brunker2022) involves defining a lineage by phylogenetic methods for tracking virus spread and comparing sequences across geographic areas, which they demonstrated with the globally distributed cosmopolitan clade of rabies virus, defining 96 total lineages within the clade. Integrating this tool with a new rabies virus sequence data resource (RABV-GLUE; http://rabv-glue.cvr.gla.ac.uk/#/home) enabled highlighting lineage dynamics relevant to control and elimination programs. In addition, ‘Outbreak analytics’ is an emerging data science focused on the technological and methodological aspects of the outbreak data. It has aided field epidemiologists in collection, visualization, and data analyses, providing decision makers with insightful information and improving our understanding of and response to outbreaks of emerging pathogens (Polonsky et al., Reference Polonsky, Baidjoe, Kamvar, Cori, Durski, Edmunds, Eggo, Funk, Kaiser, Keating, de Waroux, Marks, Moraga, Morgan, Nouvellet, Ratnayake, Roberts, Whitworth and Jombart2019).

Landscape genomics is a discipline that evaluates drivers of population structure, gene flow, and potential local adaptation and selection across the landscape. It is an approach that has been successfully used to determine dispersal in disease vectors at fine spatial scales. As an example, a study of the triatomine bug Rhodnius ecuadoriensis, a Chagas disease vector, found high-directional dispersal from forest to urban environments, as well as genomic regions likely linked to adaptations to the built environment (Hernandez-Castro et al., Reference Hernandez-Castro, Villacís, Jacobs, Cheaib, Day, Ocaña-Mayorga, Yumiseva, Bacigalupo, Andersson, Matthews, Landguth, Costales, Llewellyn and GrijalvaI2022). These findings evidenced that this triatomine bug has high capabilities to geographically disperse across multiple human communities, which jeopardizes sustainable control of Chagas disease. Importantly, readiness to predict future outbreaks and dispersal will require integration of evolutionary and epidemiological models in the context of climate, habitat, and socioeconomic modification. Among such modifications, anthropogenic perturbation and urban development prompt rapid contemporary evolutionary changes which, among others, can significantly impact transmission and the opportunity for establishment of pathogens in novel hosts (Ahmed et al., Reference Ahmed, Dávila, Allen, Haklay, Tacoli and Fèvre2019; Szulkin et al., Reference Szulkin, Munshi-South and Charmantier2020).

4. Contemporary evolutionary change: how urban development accelerates evolutionary processes

Anthropogenic perturbation and urbanization drastically transform landscapes, resulting in habitat fragmentation, degradation, and isolation, which can markedly alter dispersal and have detrimental effects on the long-term survival of populations (Mimura et al., Reference Mimura, Yahara, Faith, Vázquez-Domínguez, Colautti, Araki, Javadi, Núñez-Farfán, Mori, Zhou, Hollingsworth, Neaves, Fukano, Smith, Sato, Tachida and Hendry2017). Evolutionary change can be driven, among others, by gene flow, which is the exchange of genetic material among populations linked to the dispersal of individuals or gametes and reflecting landscape connectivity. Gene flow can impact evolutionary dynamics by fostering the maintenance of genetic diversity within populations and thus their potential to adapt to changing environments (Lambert & Donihue, Reference Lambert and Donihue2020; Richardson et al., Reference Richardson, Urban, Bolnick and Skelly2014; Tigano & Friesen, Reference Tigano and Friesen2016).

Although evolutionary change is commonly thought of as a long-term process, it is now clear that it can occur on short, ecological timescales, rendering significant changes in evolutionary traits and leading to genetic and phenotypic shifts in just a few generations (Kinnison & Hendry, Reference Kinnison and Hendry2001; Koch et al., Reference Koch, Frickel, Valiadi and Becks2014). It is now also recognized that contemporary evolution shapes ecological communities and ecosystem functions (Hendry, Reference Hendry2017; Leibold et al., Reference Leibold, Govaert, Loeuille, De Meester and Urban2022). The rapid development and growth of cities around the world can be an important driver of species' evolution (Santangelo et al., Reference Santangelo, Ness, Cohan, Fitzpatrick, Innes, Koch, Miles, Munim, Peres-Neto and Prashad2022). Indeed, urban evolution, the heritable genetic changes of populations as a response to anthropogenic activities in urban ecosystems, is one of the best and earliest examples of rapid contemporary adaptation and evolution (Kettlewell, Reference Kettlewell1955; van't Hof et al., Reference van't Hof, Campagne, Rigden, Yung, Lingley, Quail, Hall, Darby and Saccheri2016). Such evolutionary change can have both short- and long-term effects on the health and fitness of organisms (Diamond & Martin, Reference Diamond and Martin2021; Johnson & Munshi-South, Reference Johnson and Munshi-South2017; Miles et al., Reference Miles, Carlen, Winchell and Johnson2021; Szulkin et al., Reference Szulkin, Munshi-South and Charmantier2020), impact ecological dynamics of populations (Des Roches et al., Reference Des Roches, Brans, Lambert, Rivkin, Savage, Schell, Correa, De Meester, Diamond, Govaert, Harris, Hendry, Johnson, Munshi-South, Szulkin, Urban, Verrelli and Alberti2020; Lambert & Donihue, Reference Lambert and Donihue2020), and yield positive outcomes for key ecosystem services like pest control and enhancement of pollination (Lambert & Donihue, Reference Lambert and Donihue2020).

Evolution in urban environments can also have many significant negative consequences, including altered responses and spread of infectious and zoonotic diseases (Hassell et al., Reference Hassell, Begon, Ward and Fèvre2017), and the rapid evolution of invasive species (Baxter-Gilbert et al., Reference Baxter-Gilbert, Riley, Wagener, Baider, Florens, Kowalski, Campbell and Measey2022; Touchard et al., Reference Touchard, Simon, Bierne and Viard2023). Notably, genetic exchange can occur between species or between genotypes or lineages coming from different populations, and such introgressive hybridization can provide a boost in evolutionary potential (Chaturvedi et al., Reference Chaturvedi, Lucas, Buerkle, Fordyce, Forister, Nice and Gompert2020; Pacheco-Sierra et al., Reference Pacheco-Sierra, Vázquez-Domínguez, Pérez-Alquicira, Suárez-Atilano and Domínguez-Laso2018). Conversely, when exotic species are introduced outside their native range and become invasive they can lead to population declines or extinction, either due to displacement resulting from interspecific interactions (e.g. competition, predation) or through hybridization with the native species (Quilodrán et al., Reference Quilodrán, Montoya-Burgos and Currat2020). The evolution of different behavioral or reproductive traits, as well as competitive ability of invasive species, has been documented as factors facilitating range expansion and spread. For instance, the dwarf spider Mermessus trilobatus is native to North America and one of the most invasive spiders in Europe. Interestingly, dispersal behavior is highly heritable in these invasive spiders, via recessively inherited and phenotypically expressed genotypes only in offspring of two high-dispersive parents. The accumulation of dispersive genotypes in newly colonized areas and spatial selection resulting in an increase in dispersal ability has contributed to the accelerated spread of M. trilobatus in Europe (Narimanov et al., Reference Narimanov, Bauer, Bonte, Fahse and Entling2022). Evolution of such traits can play a key role in numerous arthropod invasions worldwide, with potential devastating consequences particularly in species like invasive crop pests (Nyamukondiwa et al., Reference Nyamukondiwa, Machekano, Chidawanyika, Mutamiswa, Ma and Ma2022).

Cities are associated with increased air, water, and soil pollution, and while some species can adapt to these pollutant stressors (Oziolor et al., Reference Oziolor, Reid, Yair, Lee, Guberman VerPloeg, Bruns, Shaw, Whitehead and Matson2019), others are driven to local extinction (Knapp et al., Reference Knapp, Aronson, Carpenter, Herrera-Montes, Jung, Kotze, La Sorte, Lepczyk, MacGregor-Fors, MacIvor, Moretti, Nilon, Piana, Rega-Brodsky, Salisbury, Threlfall, Trisos, Williams and Hahs2021). As such, another example of concern for sustainability is that many chemical pollutants are carcinogenic, and there is mounting evidence that multiple forms of pollution elevate cancer in humans and wild animals (Hamede et al., Reference Hamede, Owen, Siddle, Peck, Jones, Dujon, Gitaudeau, Roche, Ujvari and Thomas2020; IARC, 2016). Evolutionary concepts have been recently integrated into different forms of wildlife disease management like cancer (Hamede et al., Reference Hamede, Owen, Siddle, Peck, Jones, Dujon, Gitaudeau, Roche, Ujvari and Thomas2020), and also to understand for instance host–pathogen dynamics in non-primate humans (Solórzano-García et al., Reference Solórzano-García, Vázquez-Domínguez, Pérez Ponce de León and Piñero2021). Hence, understanding the interplay between evolutionary processes and urbanization impacts and effects is key to achieve good health and well-being, along with sustainable cities and communities.

5. Contemporary evolution and ecosystem services

Ecosystem services encompass the properties and processes through which natural ecosystems, and their constituent species, sustain human life (Daily, Reference Daily1997; Des Roches et al., Reference Des Roches, Brans, Lambert, Rivkin, Savage, Schell, Correa, De Meester, Diamond, Govaert, Harris, Hendry, Johnson, Munshi-South, Szulkin, Urban, Verrelli and Alberti2020). Evosystem services are defined as ‘all the uses or services to humans that are produced from the evolutionary process’ (Faith et al., Reference Faith, Magallón, Hendry, Conti, Yahara and Donoghue2010), coined to capture the importance of evolution for the myriad of services nature renders to people (Norgaard, Reference Norgaard2010). Given that all living organisms, and hence all ecosystem services derived from them, stem from evolution, this definition includes all ecosystem services as evosystem services (Norgaard, Reference Norgaard2010; Rudman et al., Reference Rudman, Kreitzman, Chan and Schluter2017). More recently, Rudman et al. (Reference Rudman, Kreitzman, Chan and Schluter2017) introduced the term contemporary evosystem services to explicitly address the importance of contemporary evolution to the provisioning of ecosystem services, resulting from evolution occurring quickly enough to alter ecological processes. For instance, evolutionary principles offer a novel and complementary perspective on services to humans like pollination. By considering synergies among fundamental evolutionary research, genetic engineering, and agro-ecological science, van der Niet et al. (Reference van der Niet, Egan and Schlüter2023) highlight how principles of evolutionary history of wild plant species can be applied to deal with the present pollination crisis, using technological advances to adapt crop flowers for optimal pollination by local wild pollinators, particularly by increasing generalization in pollination systems. Evolutionary concepts and tools have also been applied to control pathogens using numerical simulations of eco-evolutionary dynamics (Bargués-Ribera & Gokhale, Reference Bargués-Ribera and Gokhale2020), as well as for biocontrol of pest insects (Páez & Fleming-Davies, Reference Páez and Fleming-Davies2020).

Genetic diversity is positively associated with the provision of ecosystem services, as demonstrated by experimental restoration studies. For instance, seagrass plots with a small increase in genetic diversity harbor plants that survive longer, increase in density more quickly, and provide more services including invertebrate habitat, increased primary productivity, and nutrient retention (Reynolds et al., Reference Reynolds, McGlathery and Waycott2012). Seagrasses are key productive ecosystems engineering the maintenance of coastlines, where genetic diversity is crucial for seagrass local acclimation and adaptation in the face of climate changes (Pazzaglia et al., Reference Pazzaglia, Reusch, Terlizzi, Marín-Guirao and Procaccini2021). A decrease in species diversity and evolutionary potential, the latter caused by the loss of genetic diversity because of urbanization, habitat destruction, and habitat fragmentation, among others, strongly and negatively impact ecosystems and their associated services (Lambert & Donihue, Reference Lambert and Donihue2020). Hence, to protect and enhance the functioning of ecosystems we need to maintain the within-species genetic diversity that fuels contemporary evolution (Díaz et al., Reference Díaz, Pascual, Stenseke, Martín-López, Watson, Molnár, Hill, Chan, Baste, Brauman, Polasky, Church, Lonsdale, Larigauderie, Leadley, van Oudenhoven, van der Plaat, Schröter and Shirayama2018, Reference Díaz, Zafra-Calvo, Purvis, Verburg, Obura, Leadley, Chaplin-Kramer, De Meester, Dulloo, Martín-López, Shaw, Visconti, Broadgate, Bruford, Burgess, Cavender-Bares, DeClerck, Fernández-Palacios, Garibaldi and Zanne2020; Hughes et al., Reference Hughes, Inouye, Johnson, Underwood and Vellend2008; Molina-Venegas, Reference Molina-Venegas2021). The capacity of evolutionary processes to buffer environmental change and enhance the resilience of ecosystems also needs to be fully incorporated into sustainability science.

6. Evolution in natural and social sciences

Applied evolutionary biology and cultural evolution are key interdisciplinary approaches that intersect the natural and social sciences. Applied evolutionary biology provides a suite of strategies, from common policies that promote medicine and public health (Natterson-Horowitz et al., Reference Natterson-Horowitz, Aktipis, Fox, Gluckman, Low, Mace, Read, Turner and Blumstein2023), or preserve habitat for threatened species, to the engineering of new genomes, which help address global challenges that threaten human health, food security, and biodiversity (Carroll et al., Reference Carroll, Kinnison and Bernatchez2011, Reference Carroll, Jørgensen, Kinnison, Bergstrom, Denison, Gluckman, Smith, Strauss and Tabashnik2014). Some examples include manipulation of genetic, developmental, and environmental factors, like the genetic engineering of crops to enhance drought- and flood-tolerance. However, such strategies are easily overlooked as having an evolutionary rationale (Carroll et al., Reference Carroll, Jørgensen, Kinnison, Bergstrom, Denison, Gluckman, Smith, Strauss and Tabashnik2014). Cultural evolution integrates cultural change and variation into the theoretical framework of evolutionary science, in which cultural change and adaptation are viewed as evolutionary processes that share, but also differ in, key characteristics of genetic evolution (Boyd & Richerson, Reference Boyd and Richerson1985; Mesoudi, Reference Mesoudi2017; Pisor et al., Reference Pisor, Stephen and Kate2023). Notably, recent developments about theories of cultural evolution, niche construction, and gene-culture co-evolution are helping to bridge the gap between the study of biology, culture, and social–ecological systems (SESs) (i.e. the intersection of natural and social sciences), of which agriculture is a leading example (Altman & Mesoudi, Reference Altman and Mesoudi2019). Moreover, Currie et al. (Reference Currie, Borgerhoff, Fogarty, Schlüter, Folke, Haider, Caniglia, Tavoni, Jansen, Jørgensen and Waring2024) advise that formal evolutionary theory has rarely been applied as a dynamic theory of change of complex phenomena in SESs and propose a framework on how to integrate such dynamics of evolutionary theory into SESs. We thus fully embrace the importance of considering cultural/social evolution in furthering sustainability science, and although a more thorough consideration of these ideas is beyond the scope of our Briefing, we nonetheless encourage further readings in relevant literature (see Carroll et al., Reference Carroll, Kinnison and Bernatchez2011, Reference Carroll, Jørgensen, Kinnison, Bergstrom, Denison, Gluckman, Smith, Strauss and Tabashnik2014; Currie et al., Reference Currie, Borgerhoff, Fogarty, Schlüter, Folke, Haider, Caniglia, Tavoni, Jansen, Jørgensen and Waring2024; Pisor et al., Reference Pisor, Stephen and Kate2023).

7. Conclusion

There are many examples of the potential of evolutionary insights to contribute to key sustainability challenges like those detailed here – spread of infectious and zoonotic diseases, epidemics, ecosystem, and human health. Additionally, other contributions include food production via evolution of pesticide resistance, crop improvement by selection, genetic diversity of crop–wild relatives, water purification and soil fertility (evolution of microorganisms to efficiently remove pollutants from water bodies and to enhance nutrient cycling and soil fertility, respectively), and conservation of natural resources. Hence, as these examples show, application of evolutionary principles and tools should be integrated into crucial research for sustainability and the future of life on Earth. EvolvES, one of the Global Research Networks within Future Earth (https://futureearth.org/networks/global-researchprojects/evolves), aims to connect evolutionary biology and diversity to human well-being, stimulating collaboration between evolutionary biologists and scientists engaged in sustainability research, while raising awareness on the added value of evolutionary insights for the sustainability goals. Furthermore, among EvolvES goals is to inspire future research that explores how evolutionary expertise can be applied to find solutions that help us to achieve a sustainable future. With this Briefing we provide some insights and arguments furthering the call for a stronger collaboration between evolutionary biologists and the sustainability community. The former by increasing interdisciplinarity with sustainability research and being more active to study implications of evolutionary biology for sustainability measures and policies; and the latter by being more amenable to include natural evolutionary processes and evolutionary toolbox for decision making and development of new policies.

Acknowledgments

The content of this Briefing was developed through the Future Earth Global Research Network EvolvES, which has as its key goal to facilitate the integration of evolutionary thinking into sustainability science. Open access was obtained thanks to the Universidad Nacional Autónoma de México agreement that covers article publication charges. This paper was written in honor of Professors Mike Bruford and Louis Bernatchez, leaders in conservation genetics and inspired colleague members of the EvolvES GRN Steering Committee, whom will be greatly missed.

Author contributions

Writing of the original draft: E. V.-D., R. K., S. S., with important input from L. D. M. and M. T. J. J. All authors revised the manuscript and approved the final version.

Competing interests

None.

References

Ahmed, S., Dávila, J. D., Allen, A., Haklay, M., Tacoli, C., & Fèvre, E. M. (2019). Does urbanization make emergence of zoonosis more likely? Evidence, myths and gaps. Environment and Urbanization, 31(2), 443460. https://doi.org/10.1177/0956247819866124CrossRefGoogle ScholarPubMed
Albery, G. F., Becker, D. J., Brierley, L., Brook, C. E., Christofferson, R. C., Cohen, L. E., Dallas, T. A., Eskew, E. A., Fagre, A., Farrell, M. J., Glennon, E., Guth, S., Joseph, M. B., Mollentze, N., Neely, B. A., Poisot, T., Rasmussen, A. L., Ryan, S. J., Seifert, S., … Carlson, C. J. (2021). The science of the host–virus network. Nature Microbiology, 6, 14831492. https://doi.org/10.1038/s41564-021-00999-5CrossRefGoogle ScholarPubMed
Altman, A., & Mesoudi, A. (2019). Understanding agriculture within the frameworks of cumulative cultural evolution, gene-culture co-evolution, and cultural niche construction. Human Ecology, 47, 483497. https://doi.org/10.1007/s10745-019-00090-yCrossRefGoogle Scholar
Amicone, M., Borges, V., Alves, M. J., Isidro, J., Zé-Zé, L., Duarte, S., Vieira, L., Guiomar, R., Gomes, J. P., & Gordo, I. (2022). Mutation rate of SARS-CoV-2 and emergence of mutators during experimental evolution. Evolution, Medicine, and Public Health, 10(1), 142155. https://doi.org/10.1093/emph/eoac010CrossRefGoogle ScholarPubMed
Andersen, K. G., Rambaut, A., Lipkin, W. I., Holmes, E. C., & Garry, R. F. (2020). The proximal origin of SARS-CoV-2. Nature Medicine, 26, 450452. https://doi.org/10.1038/s41591-020-0820-9CrossRefGoogle ScholarPubMed
Bargués-Ribera, M., & Gokhale, C. S. (2020). Eco-evolutionary agriculture: Host–pathogen dynamics in crop rotations. PLoS Computational Biology, 16(1), e1007546. https://doi.org/10.1371/journal.pcbi.1007546CrossRefGoogle ScholarPubMed
Baxter-Gilbert, J., Riley, J. L., Wagener, C., Baider, C., Florens, F. B. V., Kowalski, P., Campbell, M., & Measey, J. (2022). Island hopping through urban filters: Anthropogenic habitats and colonized landscapes alter morphological and performance traits of an invasive amphibian. Animals, 12, 2549. https://doi.org/10.3390/ani12192549CrossRefGoogle ScholarPubMed
Boyd, R., & Richerson, P. J. (1985). Culture and the evolutionary process. University Chicago Press.Google Scholar
Campbell, K., Gifford, R. J., Singer, J., Hill, V., O'Toole, Á, Rambaut, A., Hampson, K., & Brunker, K. (2022). Making genomic surveillance deliver: A lineage classification and nomenclature system to inform rabies elimination. PLoS Pathogens, 18, e1010023. doi: 10.1371/journal.ppat.1010023CrossRefGoogle ScholarPubMed
Carroll, S. P., Jørgensen, P. S., Kinnison, M. T., Bergstrom, C. T., Denison, R. F., Gluckman, P., Smith, T. B., Strauss, S. Y., & Tabashnik, B. E. (2014). Applying evolutionary biology to address global challenges. Science (New York, N.Y.), 346(6207), 1245993. doi: 10.1126/science.1245993CrossRefGoogle ScholarPubMed
Carroll, S. P., Kinnison, M. T., & Bernatchez, L. (2011). In light of evolution: Interdisciplinary challenges in food, health, and the environment. Evolutionary Applications, 4, 155158. doi: 10.1111/j.1752-4571.2011.00182.xCrossRefGoogle ScholarPubMed
Chaturvedi, S., Lucas, L. K., Buerkle, C. A., Fordyce, J. A., Forister, M. L., Nice, C. C., & Gompert, Z. (2020). Recent hybrids recapitulate ancient hybrid outcomes. Nature Communications, 11, 2179. https://doi.org/10.1038/s41467-020-15641-xCrossRefGoogle ScholarPubMed
Clark, W. C., & Dickson, N. M. (2003). Sustainability science: The emerging research program. Proceedings of the National Academy of Sciences of the United States of America, 100(14), 80598061. https://doi.org/10.1073/pnas.1231333100CrossRefGoogle ScholarPubMed
Currie, T. E., Borgerhoff, M. M., Fogarty, L., Schlüter, M., Folke, C., Haider, L. J., Caniglia, G., Tavoni, A., Jansen, R. E. V., Jørgensen, P. S., & Waring, T. M. (2024). Integrating evolutionary theory and social–ecological systems research to address the sustainability challenges of the Anthropocene. Philosophical Transactions of the Royal Society B, 379, 20220262. http://doi.org/10.1098/rstb.2022.0262CrossRefGoogle ScholarPubMed
Cyrus, M. M., Bartha, I., Weaver, S., di Iulio, J., Ferri, E., Soriaga, L., Lempp, F. A., Hie, B. L., Bryson, B., Berger, B., Robertson, D. L., Snell, G., Corti, D., Virgin, H. W., Kosakovsky Pond, S. L., & Telenti, A. (2022). Predicting the mutational drivers of future SARS-CoV-2 variants of concern. Science Translational Medicine, 14, eabk3445. doi: 10.1126/scitranslmed.abk3445Google Scholar
Daily, G. C. (Ed.). (1997). Nature's services. Societal dependence on natural ecosystems. Island Press. Animal Conservation Forum, 1(1), 75–76. doi: 10.1017/S1367943098221123Google Scholar
Des Roches, S., Brans, K. I., Lambert, M. R., Rivkin, L. R., Savage, A. M., Schell, C. J., Correa, C., De Meester, L., Diamond, S. E., Govaert, L., Harris, N. C., Hendry, A. P., Johnson, M. T. J., Munshi-South, J., Szulkin, M., Urban, M. C., Verrelli, B. C., & Alberti, M. (2020). Socio-eco-evolutionary dynamics in cities. Evolutionary Applications, 14, 248267. doi: 10.1111/eva.13065CrossRefGoogle ScholarPubMed
Díaz, S., Pascual, U., Stenseke, M., Martín-López, B., Watson, R. T., Molnár, Z., Hill, R., Chan, K. M. A., Baste, I. A., Brauman, K. A., Polasky, S., Church, A., Lonsdale, M., Larigauderie, A., Leadley, P. W., van Oudenhoven, A. P. E., van der Plaat, F., Schröter, M., Lavorel, S., … Shirayama, Y. (2018). Assessing nature's contributions to people. Science (New York, N.Y.), 359, 270272. doi: 10.1126/science.aap8826CrossRefGoogle ScholarPubMed
Díaz, S., Zafra-Calvo, N., Purvis, A., Verburg, P. H., Obura, D., Leadley, P., Chaplin-Kramer, R., De Meester, L., Dulloo, E., Martín-López, B., Shaw, M. R., Visconti, P., Broadgate, W., Bruford, M. W., Burgess, N. D., Cavender-Bares, J., DeClerck, F., Fernández-Palacios, J. M., Garibaldi, L. A., … Zanne, A. E. (2020). Set ambitious goals for biodiversity and sustainability. Science (New York, N.Y.), 370, 411413. doi: 10.1126/science.abe1530CrossRefGoogle ScholarPubMed
Diamond, S. E., & Martin, R. A. (2021). Evolution in cities. Annual Review of Ecology, Evolution, and Systematics, 52, 519540.CrossRefGoogle Scholar
Exposito-Alonso, M., Booker, T. R., Czech, L., Gillespie, L., Hateley, S., Kyriazis, C. C., Lang, P. L. M., Leventhal, L., Nogues-Bravo, D., Pagowski, V., Ruffley, M., Spence, J. P., Toro Arana, S. E., Weiß, C. L., & Zess, E. (2022). Genetic diversity loss in the Anthropocene. Science (New York, N.Y.), 377(6613), 14311435. https://doi.org/10.1126/science.abn5642CrossRefGoogle ScholarPubMed
Faith, D. P., Magallón, S., Hendry, A. P., Conti, E., Yahara, T., & Donoghue, M. J. (2010). Evosystem services: An evolutionary perspective on the links between biodiversity and human well-being. Current Opinion in Environmental Sustainability, 2, 6674.CrossRefGoogle Scholar
Gandon, S., Day, T., Metcalf, C. J. E., & Grenfell, B. T. (2016). Forecasting epidemiological and evolutionary dynamics of infectious diseases. Trends in Ecology & Evolution, 31, 776788.CrossRefGoogle ScholarPubMed
Good, B. H., McDonald, M. J., Barrick, J. E., Lenski, R. E., & Desai, M. M. (2017). The dynamics of molecular evolution over 60,000 generations. Nature, 551, 4550. https://doi.org/10.1038/nature24287CrossRefGoogle Scholar
Grubaugh, N. D., Ladner, J. T., Lemey, P., Pybus, O. G., Rambaut, A., Holmes, E. C., & Andersen, K. G. (2019). Tracking virus outbreaks in the twenty-first century. Nature Microbiology, 4, 1019.CrossRefGoogle ScholarPubMed
Hamede, R., Owen, R., Siddle, H., Peck, S., Jones, M., Dujon, A. M., Gitaudeau, M., Roche, B., Ujvari, B., & Thomas, F. (2020). The ecology and evolution of wildlife cancers: Applications for management and conservation. Evolutionary Applications, 13, 17191732. https://doi.org/10.1111/eva.12948CrossRefGoogle ScholarPubMed
Hassell, J. M., Begon, M., Ward, M. J., & Fèvre, E. M. (2017). Urbanization and disease emergence: Dynamics at the wildlife–livestock–human interface. Trends in Ecology and Evolution, 32(1), 5567. doi: 10.1016/j.tree.2016.09.012CrossRefGoogle ScholarPubMed
Hendry, A. P. (2017). Eco-evolutionary dynamics. Princeton University Press.CrossRefGoogle Scholar
Hernandez-Castro, L. E., Villacís, A. G., Jacobs, A., Cheaib, B., Day, C. C., Ocaña-Mayorga, S., Yumiseva, C. A., Bacigalupo, A., Andersson, B., Matthews, L., Landguth, E. L., Costales, J. A., Llewellyn, M. S., & GrijalvaI, M. J. (2022). Population genomics and geographic dispersal in Chagas disease vectors: Landscape drivers and evidence of possible adaptation to the domestic setting. PLoS Genetics, 18(2), e1010019. https://doi.org/10.1371/journal.pgen.1010019CrossRefGoogle Scholar
Hill, V., & Rambaut, A. (2020). Phylodynamic analysis of SARS-CoV-2. Update 2020-03-06.Google Scholar
Hughes, A. R., Inouye, B. D., Johnson, M. T. J., Underwood, N., & Vellend, M. (2008). Ecological consequences of genetic diversity. Ecology Letters, 11(6), 609623. https://doi.org/10.1111/j.1461-0248.2008.01179.xCrossRefGoogle ScholarPubMed
IARC Working Group on the Evaluation of Carcinogenic Risks to Humans (2016). Outdoor air pollution. IARC Monographs on the Identification of Carcinogenic Hazards to Humans, 109, 9444.Google Scholar
Johnson, M. T. J., & Munshi-South, J. (2017). Evolution of life in urban environments. Science (New York, N.Y.), 358(6363), eaam8327. https://doi.org/10.1126/science.aam8327CrossRefGoogle ScholarPubMed
Kassen, R. (2019). Experimental evolution of innovation and novelty. Trends in Ecology & Evolution, 34, 712722.CrossRefGoogle ScholarPubMed
Kettlewell, H. B. D. (1955). Selection experiments on industrial melanism in the Lepidoptera. Heredity, 9, 323342.CrossRefGoogle Scholar
Kinnison, M. T., & Hendry, A. P. (2001). The pace of modern life II: From rates of contemporary microevolution to pattern and process. Genetica, 112-113, 145164.CrossRefGoogle ScholarPubMed
Knapp, S., Aronson, M. F. J., Carpenter, E., Herrera-Montes, A., Jung, K., Kotze, D. J., La Sorte, F. A., Lepczyk, C. A., MacGregor-Fors, I., MacIvor, J. S., Moretti, M., Nilon, C. H., Piana, M. R., Rega-Brodsky, C. C., Salisbury, A., Threlfall, C. G., Trisos, C., Williams, N. S. G., & Hahs, A. K. (2021). A research agenda for urban biodiversity in the global extinction crisis. BioScience, 71, 268279. https://doi.org/10.1093/biosci/biaa141CrossRefGoogle Scholar
Koch, H., Frickel, J., Valiadi, M., & Becks, L. (2014). Why rapid, adaptive evolution matters for community dynamics. Frontiers in Ecology and Evolution, 2, 17. doi: 10.3389/fevo.2014.00017CrossRefGoogle Scholar
Lambert, M. R., & Donihue, C. M. (2020). Urban biodiversity management using evolutionary tools. Nature Ecology and Evolution, 4, 903910. https://doi.org/10.1038/s41559-020-1193-7CrossRefGoogle ScholarPubMed
Leibold, M. A., Govaert, L., Loeuille, N., De Meester, L., & Urban, M. C. (2022). Evolution and community assembly across spatial scales. Annual Review of Ecology, Evolution, and Systematics, 53, 299326.CrossRefGoogle Scholar
Li, X., Zai, J., Zhao, Q., Nie, Q., Li, Y., Foley, B. T., & Chaillon, A. (2020). Evolutionary history, potential intermediate animal host, and cross-species analyses of SARS-CoV-2. Journal of Medical Virology, 92, 602611.CrossRefGoogle ScholarPubMed
Mesoudi, A. (2017). Pursuing Darwin's curious parallel: Prospects for a science of cultural evolution. Proceedings of the National Academy of Sciences of the United States of America, 114(30), 78537860. https://doi.org/10.1073/pnas.1620741114CrossRefGoogle ScholarPubMed
Messerli, P., Kim, E. M., Lutz, W., Moatti, J.-P., Richardson, K., Saidam, M., Smith, D., Eloundou-Enyegue, P., Foli, E., Glassman, A., Licona, G. H., Murniningtyas, E., Staniškis, J. K., van Ypersele, J.-P., & Furman, E. (2019). Expansion of sustainability science needed for the SDGs. Nature Sustainability, 2(10), 892894. https://doi.org/10.1038/s41893-019-0394-zCrossRefGoogle Scholar
Miles, L. S., Carlen, E. J., Winchell, K. M., & Johnson, M. T. J. (2021). Urban evolution comes into its own: Emerging themes and future directions of a burgeoning field. Evolutionary Applications, 14(1), 311. https://doi.org/10.1111/eva.13165CrossRefGoogle ScholarPubMed
Mimura, M., Yahara, T., Faith, D. P., Vázquez-Domínguez, E., Colautti, R. I., Araki, H., Javadi, F., Núñez-Farfán, J., Mori, A. S., Zhou, S., Hollingsworth, P. M., Neaves, L. E., Fukano, Y., Smith, G., Sato, Y.-I., Tachida, H., & Hendry, A. P. (2017). Understanding and monitoring the consequences of human impacts on intraspecific variation. Evolutionary Applications, 10, 121139.CrossRefGoogle ScholarPubMed
Molina-Venegas, R. (2021). Conserving evolutionarily distinct species is critical to safeguard human well-being. Scientific Reports, 11(1), 24187. https://doi.org/10.1038/s41598-021-03616-xCrossRefGoogle ScholarPubMed
Naderi, S., Chen, P. E., Murall, C. L., Poujol, R., Kraemer, S., Pickering, B. S., Sagan, S. M., & Shapiro, B. J. (2023). Zooanthroponotic transmission of SARS-CoV- 2 and host-specific viral mutations revealed by genome-wide phylogenetic analysis. eLife, 12, e83685. https://doi.org/10.7554/eLife.83685CrossRefGoogle ScholarPubMed
Narimanov, N., Bauer, T., Bonte, D., Fahse, L., & Entling, M. H. (2022). Accelerated invasion through the evolution of dispersal behaviour. Global Ecology and Biogeography, 31, 24232436. https://doi.org/10.1111/geb.13599CrossRefGoogle Scholar
Natterson-Horowitz, B., Aktipis, A., Fox, M., Gluckman, P. D., Low, F. M., Mace, R., Read, A., Turner, P. E., & Blumstein, D. T. (2023). The future of evolutionary medicine: Sparking innovation in biomedicine and public health. Frontiers in Science, 1, 997136. doi: 10.3389/fsci.2023.997136CrossRefGoogle ScholarPubMed
Norgaard, R. B. (2010). Ecosystem services: From eye-opening metaphor to complexity blinder. Ecological Economics, 69, 12191227. https://doi.org/10.1016/j.ecolecon.2009.11.009CrossRefGoogle Scholar
Nyamukondiwa, C., Machekano, H., Chidawanyika, F., Mutamiswa, R., Ma, G., & Ma, C. S. (2022). Geographic dispersion of invasive crop pests: The role of basal, plastic climate stress tolerance and other complementary traits in the tropics. Current Opinion in Insect Science, 50, 100878. https://doi.org/10.1016/j.cois.2022.100878CrossRefGoogle ScholarPubMed
Obermeyer, F., Jankowiak, M., Barkas, N., Schaffner, S. F., Pyle, J. D., Yurkovetskiy, L., Bosso, M., Park, D. J., Babadi, M., Macinnis, B. L., Luban, J., Sabeti, C., & Lemieux, J. E. (2022). Analysis of 6.4 million SARS-CoV-2 genomes identifies mutations associated with fitness. Science (New York, N.Y.), 376, 13271332. https://doi.org/10.1126/science.abm1208CrossRefGoogle ScholarPubMed
Oziolor, E. M., Reid, N. M., Yair, S., Lee, K. M., Guberman VerPloeg, S., Bruns, P. C., Shaw, J. R., Whitehead, A., & Matson, C. W. (2019). Adaptive introgression enables evolutionary rescue from extreme environmental pollution. Science (New York, N.Y.), 364, 455457.CrossRefGoogle ScholarPubMed
Pacheco-Sierra, G., Vázquez-Domínguez, E., Pérez-Alquicira, J., Suárez-Atilano, M., & Domínguez-Laso, J. (2018). Ancestral hybridization yields evolutionary distinct hybrids lineages and species boundaries in crocodiles, posing unique conservation conundrums. Frontiers in Ecology and Evolution, 6, 138.CrossRefGoogle Scholar
Páez, D., & Fleming-Davies, A. (2020). Understanding the evolutionary ecology of host–pathogen interactions provides insights into the outcomes of insect pest biocontrol. Viruses, 12(2), 141. doi: 10.3390/v12020141CrossRefGoogle ScholarPubMed
Pazzaglia, J., Reusch, T. B. H., Terlizzi, A., Marín-Guirao, L., & Procaccini, G. (2021). Phenotypic plasticity under rapid global changes: The intrinsic force for future seagrasses survival. Evolutionary Applications, 14(5), 11811201. https://doi.org/10.1111/eva.13212CrossRefGoogle ScholarPubMed
Pisor, A., Stephen, L. J., & Kate, M. (2023). Climate change adaptation needs a science of culture. Philosophical Transactions of the Royal Society B, 378, 20220390. http://doi.org/10.1098/rstb.2022.0390CrossRefGoogle Scholar
Polonsky, J. A., Baidjoe, A., Kamvar, Z. N., Cori, A., Durski, K., Edmunds, W. J., Eggo, R. M., Funk, S., Kaiser, L., Keating, P., de Waroux, O. L. P., Marks, M., Moraga, P., Morgan, O., Nouvellet, P., Ratnayake, R., Roberts, C. H., Whitworth, J., & Jombart, T. (2019). Outbreak analytics: A developing data science for informing the response to emerging pathogens. Philosophical Transactions of the Royal Society B, 374(1776), 20180276. doi: 10.1098/rstb.2018.0276CrossRefGoogle ScholarPubMed
Quilodrán, C. S., Montoya-Burgos, J. I., & Currat, M. (2020). Harmonizing hybridization dissonance in conservation. Communications Biology, 3, 391. https://doi.org/10.1038/s42003-020-1116-9CrossRefGoogle ScholarPubMed
Randolph, S. E., & Rogers, D. J. (2010). The arrival, establishment and spread of exotic diseases: Patterns and predictions. Nature Review Microbiology, 8, 361371.CrossRefGoogle ScholarPubMed
Reynolds, L. K., McGlathery, K. J., & Waycott, M. (2012). Genetic diversity enhances restoration success by augmenting ecosystem services. PLoS ONE, 7(6), e38397. doi: 10.1371/journal.pone.0038397CrossRefGoogle ScholarPubMed
Richardson, J. L., Urban, M. C., Bolnick, D. I., & Skelly, D. K. (2014). Microgeographic adaptation and the spatial scale of evolution. Trends in Ecology & Evolution, 29, 165176.CrossRefGoogle ScholarPubMed
Rudman, S. M., Kreitzman, M., Chan, K. M. A., & Schluter, D. (2017). Evosystem services: Rapid evolution and the provision of ecosystem services. Trends in Ecology & Evolution, 32(6), 403415. https://doi.org/10.1016/j.tree.2017.02.019CrossRefGoogle ScholarPubMed
Santangelo, J. S., Ness, R. W., Cohan, B., Fitzpatrick, C. R., Innes, S. G., Koch, S., Miles, L. S., Munim, S., Peres-Neto, P. R., & Prashad, C. (2022). Global urban environmental change drives adaptation in white clover. Science (New York, N.Y.), 375(6586), 12751281.CrossRefGoogle ScholarPubMed
Singh, D., & Yi, S. V. (2021). On the origin and evolution of SARS-CoV-2. Experimental & Molecular Medicine, 53, 537547. https://doi.org/10.1038/s12276-021-00604-zCrossRefGoogle ScholarPubMed
Smith, K. F., Goldberg, M., Rosenthal, S., Carlson, L., Chen, J., Chen, C., & Ramachandran, S. (2014). Global rise in human infectious disease outbreaks. Journal of the Royal Society Interface, 11, 20140950. https://doi.org/10.1098/rsif.2014.0950CrossRefGoogle ScholarPubMed
Solórzano-García, B., Vázquez-Domínguez, E., Pérez Ponce de León, G., & Piñero, D. (2021). Co-structure analysis and genetic associations reveal insights into pinworms (Trypanoxyuris) and primates (Alouatta palliata) microevolutionary dynamics. BMC Ecology and Evolution, 21, 190. https://doi.org/10.1186/s12862-021-01924-4CrossRefGoogle ScholarPubMed
Szulkin, M., Munshi-South, J., & Charmantier, A. (2020). Urban evolutionary biology. Oxford University Press.CrossRefGoogle Scholar
Tigano, A., & Friesen, V. L. (2016). Genomics of local adaptation with gene flow. Molecular Ecology, 25, 21442164.CrossRefGoogle ScholarPubMed
Touchard, F., Simon, A., Bierne, N., & Viard, F. (2023). Urban rendezvous along the seashore: Ports as Darwinian field labs for studying marine evolution in the Anthropocene. Evolutionary Applications, 16, 560579. https://doi.org/10.1111/eva.13443CrossRefGoogle ScholarPubMed
van der Niet, T., Egan, P. A., & Schlüter, P. M. (2023). Evolutionarily inspired solutions to the crop pollination crisis. Trends in Ecology & Evolution, 38(5), 435445. https://doi.org/10.1016/j.tree.2022.12.010CrossRefGoogle Scholar
van't Hof, A. E., Campagne, P., Rigden, D. J., Yung, C. J., Lingley, J., Quail, M. A., Hall, N., Darby, A. C., & Saccheri, I. J. (2016). The industrial melanism mutation in British peppered moths is a transposable element. Nature, 53, 102105.CrossRefGoogle Scholar
Visher, E., Evensen, C., Guth, S., Lai, E., Norfolk, M., Rozins, C., Sokolov, N. A., Sui, M., & Boots, M. (2021). The three Ts of virulence evolution during zoonotic emergence. Proceedings of the Royal Society B, 288, 20210900.CrossRefGoogle ScholarPubMed