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).