Human‐induced evolution: Signatures, processes and mechanisms underneath anthropogenic footprints on natural systems

Abstract The impact of human activities on the global environment has increased to such an extent that the current geological era has been coined the Anthropocene. Studies dedicated to understanding the evolutionary consequences of human‐induced selection on all levels of diversity (species, populations, traits, genes) provide direct knowledge about the mechanisms underlying species' responses and their evolutionary potential. A better understanding of the effects of human‐induced selection is needed to leverage evolved mechanisms to develop appropriate conservation programmes to guarantee the maintenance of healthy systems. In this special issue, we focus on different types of human‐mediated selection pressures, from the direct harvesting of individuals (e.g. hunting, fishing), to the more pervasive effects of climate change. Contributions highlight the diversity of human‐induced selection pressures ranging from fisheries, trophy‐hunting, poaching and domestication to climate change, and pollution. With those, we question whether there are parallel evolutionary solutions across fisheries systems, whether hunting pressures alter population dynamics and population structure, and whether climate change is an evolutionary dead‐end. The contributions reflect the direction of travel of the field and the solutions to mitigate the impact of human activities.


| INTRODUC TI ON
Earth's geological timescale has been historically defined by natural events that substantially transformed the global environment (Lewis & Maslin, 2015). Transitions, such as those marking the Permian-Triassic boundary or the Cretaceous-Paleogene boundary, are geologically established events of our planet's history characterized by extensive change in the Earth's biota (Erwin, 1998;Jablonski, 1986).
Nowadays, it is widely acknowledged that the exponential increase of human activities has had a comparable impact, and as such, the current times have been coined the Anthropocene (Ceballos et al., 2015;Crutzen & Stoermer, 2000;Lewis & Maslin, 2015).
Anthropogenically driven environmental impacts encompass, for instance, pronounced changes in biogeochemistry such as the alteration of the carbon cycle because of excessive burning of fossil fuel into the atmosphere, enhancing greenhouse effects (IPCC, 2021;Raupach & Canadell, 2010;Summerhayes & Zalasiewicz, 2018;Vitousek et al., 1997). Specifically to biological systems, human activities have caused a series of local extinctions and the selective extirpation of large-bodied animals from terrestrial and marine environments (Barnosky et al., 2011;Turvey & Crees, 2019). Arguably, human-mediated selection constitutes one of the greatest and most pervasive selective forces on Earth (Hendry et al., 2017;Palumbi, 2001) changing at a pace that requires rapid evolution of adaptive responses.
This Special Issue stems from a symposium we organized at the 2019 European Society of Evolutionary Biology (ESEB) meeting in Turku, Finland, that focused on detailing the emergence of evolutionary responses to a broad range of human activities. Here, we expanded the scope to include a set of timely reviews and perspectives. The overarching goal of this Special Issue is to beacon discussions and raise awareness on scenarios of human-induced evolution, state-of-the-art methods and overall strategies to understand and characterize signatures of human-induced evolution.
Here, we define human-induced evolution as emergent evolutionary changes either on heritable traits or on their genetic and epigenetic basis as responses to direct or indirect pressures imposed by human activities. Among the earlier and better-established examples of human-induced selection for desirable traits is animal and plant domestication, which has enabled the transition from nomadic hunter-gathering societies to a sedentary, agriculture-based, livelihood (Goudie, 2018). Overall, our socio-economic development is intertwined with increasing pressures on the environment, ranging from local or regional effects, such as shaping river courses during the Bronze Age, to more global impacts, such as fossil fuel combustion that prompted the Industrial Revolution (Leigh et al., 2019;Zalasiewicz et al., 2011). Because contemporary anthropogenic activities impose strong ecological selective pressures, there are arguably more suitable scenarios to observe real-time evolution in natural settings than environments disturbed by human activities.
Identifying evolutionary responses fuelled by our actions, including the quantification of their magnitude across space and time, is critical to estimate long-term consequences of human-induced evolution on biodiversity and ecosystem functioning (Lambert & Donihue, 2020).
Understanding the processes underlying evolutionary responses will also facilitate the development of appropriate mitigation strategies to reduce detrimental impacts of human activities on natural systems (Ottenburghs, 2021).

| Human-induced evolution as natural experiments
Translocations, defined as the active transport of specimens across geographically unconnected areas, is representative of the human ability to manipulate migration and gene flow (Heckwolf et al., 2021).
In the past, translocations were necessary operations to maintain the comfort necessary to flourishing societies, such as the transport of domesticated dogs from the Old to the New World (Hofman & Rick, 2018). Currently, those activities are performed with different objectives that may range from restoring biodiversity of depleted habitats, as pest controls, or simply to enhance the aesthetics of urbanized areas. In the context of a conservation effort of whitefish species (Coregonus sp.) in Scottish lakes, Crotti et al. (2021) investigated six recently man-made whitefish populations that originated from a translocation event to boost these fish's abundances. Results point out an overall lower genomic diversity and higher inbreeding among translocated populations were also associated with a high degree of differentiation among original and translocated populations. Differentiation was observed for (a) eco-morphological traits associated with body shape, (b) DNA methylation patterns and (c) SNPs that revealed genomic selection in response to translocations.
Overall, the species' evolutionary potential is apparently sufficient to overcome genetic bottlenecks (Crotti et al., 2021). The holistic approach undertook by Crotti et al. is the one needed to quantify the evolutionary potential of such species (Eizaguirre & Baltazar-Soares, 2014). Another sort of human-mediated species' movement relates to biological organisms that hold a symbiotic relationship with humans via domestication. The establishment and expansion of human settlements provide the opportunity for secondary contact between domesticated species and their wild counterparts (Ottenburghs, 2021). If reproductive isolation is incomplete, then hybridization between domesticated and wild species can occur (Grabenstein & Taylor, 2018;Hamilton & Miller, 2016). Capturing signatures of hybridization events is critical to maintain the integrity of wild specimens in the ever-expanding era of the Anthropocene (Ottenburghs, 2021). In this context, genome scans are useful to reveal signatures of human-driven hybridization as those can identify introgression patterns among admixed populations of domesticated and wild species (Pilot et al., 2021). Introgression from free-ranging domestic dogs into populations of Eurasian wolves for example has shown that the transfer of genetic material might reduce Eurasian's wolf viability by genetic swamping. This effect further impact genetic diversity that is already negatively affected by genetic drift associated with small population sizes resulting from hunting and habitat loss (Pilot et al., 2021). The study provides new perspective to address conservation efforts of wolf's genetic integrity; namely, it advocates the maintenance of large population sizes as an important measure of management strategies in order to avoid swamping by dog-derived variants in wolf's genome (Pilot et al., 2021). Because of the longstanding contact and dependence on human activities, farmed animals might pose a similar risk to natural populations upon reproduction with wild animals (Le Luyer et al., 2017;Leitwein et al., 2021). Hence, it is critical to identify and characterize hypothetical marks of human-induced selection and whenever possible the effects on fitness-related traits. Utilizing a whole genome bisulphite sequencing approach, Leitwein et al. (2021) showed that hatcheryreared Coho salmon (Oncorhynchus kisutch) exhibit a distinct epigenetic make-up, both at a chromosomal and at a localized level, from those born in the wild despite being genetically indistinguishable.
The fact that those epigenetic marks persist through adulthood in germline cells opens room for transgenerational inheritance and the potential spread of human-induced signatures among wild populations.
Overall, the prevalence of anthropogenic hybridization that threatens the viability of wild populations calls for more efforts in exploring and predicting the evolutionary trajectories and outcome of hybridization (McFarlane et al., 2020). Ottenburghs (2021) summarizes the state of the art in this field and calls for speciation genomics specialists to focus on past hybridization events to predict introgression patterns among recently interbred species. Genomewide scans associated with mapping into annotated reference genomes can enable identifying the genomic regions primarily introgressed, revolutionizing the development of diagnostic genetic markers underlying functional traits (Ottenburghs, 2021).

| Antagonistic effects of human-induced selection on behaviour and life history and impacts to population dynamics
In contrast to translocations or anthropogenic hybridization, harvesting activities such as hunting, or fishing exert a predictable selection because its strong intensity and direction are largely dictated by specific harvesting strategies (Allendorf & Hard, 2009;Hočevar & Kuparinen, 2021;Van de Walle et al., 2021).
Consequently, harvesting re-shapes selection regimes that populations have adapted to and can result in antagonistic phenotypic responses of fitness-related life history traits (Heino et al., 2015;LaSharr et al., 2019). For instance, the use of nets with specific mesh size and standardized hook size renders fishing a sizeselection experiment that promotes faster development rates, thus selecting for early age at maturation (Hutchings & Kuparinen, 2020). Similarly, hunting of bighorn sheep (Ovis canadensis) with large horn size imposes a gradual reduction of male horn length, a secondary sexual trait (Pigeon et al., 2016). While our knowl- Human-induced responses that contrast those that emerged through natural selection are not exclusive to harvesting regimes.
By investigating the effect of increased algal turbidity, Candolin et al. (2021) found that courtship behaviour of male sticklebacks (Gasterosteus aculeatus) is highly plastic and exposed to differential selection under eutrophic conditions. However, most of the plasticity appears to be maladaptive: turbid conditions lead males to spend more time by the nest, contrary to female preferred behaviour such as increased search activity and time spent by the female. Comparable changes in behaviours during the reproductive period were also observed in sea turtles (Caretta caretta) nesting in Zakynthos (Greece), whereby the presence of tourists forces the turtles to use suboptimal, slightly cooler waters, that slow-down egg development (Schofield et al., 2021). The impact is a likely longer nesting period, which may result in lower hatching success, ultimately selecting for faster development with unknown consequences. The forced displacement of turtles was only visible because of the ban on travel related to the SARS-CoV2 pandemic, which reduced the effects of tourist presence on turtle behaviours (Schofield et al., 2021).
Observations that anthropogenic actions exert a selective pressure in the opposite direction of natural selection implies that management strategies undertaken to mitigate human-induced evolution should consider possible trade-offs in populations already adapted to human pressure (Hočevar & Kuparinen, 2021;Van de Walle et al., 2021). Given that the reversibility of evolutionary changes remains largely unknown, it is perhaps advisable to acknowledge factors such as the heterogeneity of selective pressures across spatial and temporal scales prior to the implementation of uniform measures.

| Pollution and multistressor environments of urbanized areas
Because of the immediate impact on the fitness and health of organisms, pollution is considered one of the major contributors of humaninduced evolution . Mining, fossil fuel usage and large-scale application of pesticides release excessive amounts of nondegradable pollutants into the environment, both terrestrial and aquatic. High concentrations of chemicals or heavy metals disrupt metabolic pathways and biological functions, and as such, the pressure imposed is direct and directional for increasing tolerance. With that in mind, Calboli et al. (2021) performed a genome-wide association study to investigate the genetic basis of mercury tolerance in sticklebacks (Gasterosteus aculeatus) collected along a gradient of polluted environments. Exploring an association between mercury in muscle tissue and genome-wide genomic variants, Calboli et al. found localized genomic regions putatively involved in adaptation to mercury-polluted environments. The study further identified outlier loci in regions known to be involved in spacing of pharyngeal teeth, probably suggesting a functional adaptive link, whether direct or indirect, between diet and pollution. While a strong selective pressure, pollution is seldom the unique stressor to which organismal populations of urbanized areas are subjected to . Through the exposure of clonal lineages of urban and rural Daphnia magna populations to acute toxicity (organophosphate pesticide chlorpyrifos) at two temperatures, Brans et al. (2021) showed that urban water flea populations have higher survival probabilities, independent of temperature regimes compared to those from rural origin. Resistance against toxic agents suggests the evolution of an adaptive response that could ultimately hinder pest-control strategies and facilitate persistence of these organisms in urbanized environments. Because human impacts are relatively recent, reviving dormant stages of organisms collected from pristine environments prior the exposure to intense selection offer an interesting perspective to characterize evolutionary trajectories of those species (Weider et al., 2018). It can inform on timing of the response as well as the tolerance to variable selection pressure. By performing experiments on resurrected Daphnia populations that were either naïve or exposed to human impacts over time, Cuenca-Cambronero et al.
(2021) explored whether and how chemical pollution and eutrophication triggered adaptive responses. Results showed that the emergence of adaptive responses to multiple human-induced stressors comes with added selection in the form of increased mortality and reduced fertility (Cuenca-Cambronero et al., 2021).
In general, pollution is an added selection pressure to those already experienced by natural populations. Like many others, the intensification of human activities creates a directional selection pressure that species need to cope with. Whether the pace of the response is sufficient to enable their persistence is still unknown but hints that with a sufficiently large population size, gene flow and well-managed policy programme, positive outcome are possible.

| The impact of anthropogenic climate changeshifts on species distributions and connectivity
Temperature has been one of the most significant mediators of species' diversity and distribution on Earth over geological times.
We now know that shifts either in temperature or in temperaturedependent environmental variables have been involved in largescale extinction events, or in changes in distribution via retractions/ expansions during the Quaternary's glacial cycles (Hewitt, 2000;Penn et al., 2018). With temperatures rising at unprecedented pace, anthropogenic climate change is bound to dictate large shifts in the distribution of contemporary organisms (Rosenzweig et al., 2008).
Modelling distribution shifts is thus an active area of research that represents one possibility to predict responses of certain species.
Among others, implications of a climate change scenario extend to intrinsic biological processes, such as phenology-related aspects of flowering plant's life cycles, insects life history, or bird massive migration mediated by seasonality. Here, Lockley and Eizaguirre (2021) reflects over the impacts of anthropogenic climate change on species whose sex is determined by temperature. Temperaturedependent sex determination (TSD) exists in over 400 species, where the incubation temperature mediates gonad development. Lockley and Eizaguirre (2021) reviewed the specific literature to explore predictions that under fast-paced changing climate scenarios, TSD species might be confronted with skewed sex ratios and risk extinction if evolutionary responses do not emerge as quickly as temperature shifts (Lockley & Eizaguirre, 2021). Yet, they also uphold the suggestion that since species with TSD have experienced large-scale climatic events across their evolutionary history, the species must have evolved mechanisms that buffer sex ratio bias, further, suggesting that maternal hormone transfer enables to resist the developmental transition from male to female in sea turtles as temperature increases. Jointly with evolutionary responses, the ability for depauperated populations to recover from environmental disturbances depends on the availability of migrants from unaffected locations. Reef systems are particularly vulnerable to climate change, with thermal stress causing bleaching events that might occur at very localized scales (Afiq-Rosli et al., 2021). Hence, characterizing the connectivity across large geographic scales is critical to identify potential source populations and eventually perform restoration activities. Afiq-Rosli et al. (2021) exemplified just that in a study that comprised the screen of over 30k SNPs obtained with NextRAD from nine populations of reef-building corals (Porites sp. and Pocillopora acuta). The identification of fine-scale population structure might provide solutions for management strategies that aim to repopulate bleached systems.
Overall, studies investigating the effects of climate change need to consider many elements. Firstly, species have survived past climatic events and therefore may have evolved still unknown mechanisms, which contribute to a species' evolutionary potential. This calls for mechanistic studies to contribute to studying the effect of climate change. Secondly, species may evolve partial tolerance to changes and species distribution shift need to consider that species may look for suboptimal conditions. Lastly, there is a clear role for evolutionary biologists to play to guide conservation efforts to leverage natural mechanisms to manage populations.

| Evolutionary applications in the Anthropocene
The global impact of anthropogenic activities is likely to influence

ACK N OWLED G M ENTS
We would like to thank all of those who contributed to the symposium "Human-induced evolution" at the ESEB2019. We would also like to thank the Evolutionary Applications editorial team, in particular Prof. Louis Bernatchez, for the opportunity to compile relevant contributions to the field into a Special Issue.

CO N FLI C T O F I NTE R E S T S
The authors declare no conflict of interest.

DATA AVA I L A B I L I T Y S TAT E M E N T
Does not apply to this manuscript.