An evolutionary perspective on marine invasions

Abstract Species distributions are rapidly changing as human globalization increasingly moves organisms to novel environments. In marine systems, species introductions are the result of a number of anthropogenic mechanisms, notably shipping, aquaculture/mariculture, the pet and bait trades, and the creation of canals. Marine invasions are a global threat to human and non‐human populations alike and are often listed as one of the top conservation concerns worldwide, having ecological, evolutionary, and social ramifications. Evolutionary investigations of marine invasions can provide crucial insight into an introduced species’ potential impacts in its new range, including: physiological adaptation and behavioral changes to exploit new environments; changes in resident populations, community interactions, and ecosystems; and severe reductions in genetic diversity that may limit evolutionary potential in the introduced range. This special issue focuses on current research advances in the evolutionary biology of marine invasions and can be broadly classified into a few major avenues of research: the evolutionary history of invasive populations, post‐invasion reproductive changes, and the role of evolution in parasite introductions. Together, they demonstrate the value of investigating marine invasions from an evolutionary perspective, with benefits to both fundamental and applied evolutionary biology at local and broad scales.


| INTRODUC TI ON
Species distributions are rapidly changing, facilitated by enhanced human migration and globalization over the past several centuries.
Increasingly, species are becoming introduced to and established in novel locations that are often well outside their limits for natural dispersal. In marine systems, the anthropogenic transfer of living organisms has occurred as a result of multiple mechanisms including shipping, aqua-or mariculture, pet trade, bait trade, food trade, and canals. Marine invasions represent a global threat to human populations and broader biological communities and are often listed as one of the top conservation concerns worldwide (IPCC, 2019). As species continue to expand along the coasts and within estuaries, they can have devastating environmental and socioeconomic impacts (Lovell, Stone, & Fernandez, 2006;Bennett, 2018;Giakoumi et al., 2019). Some notable examples include the lionfish Pterois miles, the puffer fish Lagocephalus sceleratus, the ctenophore Mnemiopsis leidyi, the European green crab Carcinus maenas, the round goby Neogobius melanostomus, and the green alga Caulerpa taxifolia. Invasive species can spread rapidly, successfully colonizing and expanding their ranges within a matter of years to decades (e.g., Azzurro, Soto, Garofalo, & Maynou, 2012). In the process, they introduce multiple novel interactions to land and seascapes over a potentially vast new range. Some species may have disproportionately strong effects on their invaded communities, such as habitat-forming species that greatly alter landscapes postinvasion, for example, global invasions of the macroalga Agarophyton vermiculophyllum (formerly Gracilaria vermiculophylla) and the Pacific oyster Crassostrea gigas. Both add novel structure to soft-sediment habitats (e.g., Krueger-Hadfield, Stephens, Ryan, & Heiser, 2018;Reise, 1998;Thomsen et al., 2007;Troost, 2010). Actions that prevent species establishments before they occur are necessary to avoid the destructive damage invasive species can cause: Postestablishment measures to control invasive species often fail and are incredibly costly. However, these preventative strategies can be expensive and impractical, particularly for developing nations (Lodge et al., 2006). Moreover, national strategic planning for marine invasions is globally diverse and typically lacks unified policies across and even within nations (Keller, Geist, Jeschke, & Kühn, 2011). Consequently, rates of anthropogenic transport have continued to increase worldwide, as has the spread and expansion of many species that would otherwise be geographically constrained.
Prevention and control efforts often focus on the ecological and economic harm associated with an invasive species, while the possible evolutionary ramifications of a species invasion are typically overlooked. Yet, investigating marine invasions from an evolutionary perspective can provide crucial insight into an introduced species' potential influence in its invasive range (Geller, Darling, & Carlton, 2010;Grosholz, 2002;Hänfling, 2007).
Evolutionary changes can be rapid and varied, including physiological adaptation and behavioral changes to exploit new environments (Lee, Posavi, & Charmantier, 2012;Piola & Johnston, 2006;Tepolt & Somero, 2014). Likewise, resident species may evolve quickly in response to strong selective forces exerted by invaders, leading to changes in resident populations, community interactions, and even the broader environment (Edgell, Lynch, Trussell, & Palmer, a R., 2009;Faillace & Morin, 2016;Hollander & Bourdeau, 2016). Nonselective forces may also be at play, with the potential for severe reductions in genetic diversity associated with species invasions that influence the resulting genotypic composition in the introduced range (Roman & Darling, 2007). Invasive species may interbreed with native congeners, diluting native genomes and potentially overwhelming evolutionarily novel lineages (Gardner, Zbawicka, Westfall, & Wenne, 2016;Strong & Ayres, 2013). To date, determining how invasion dynamics and species interactions impact evolutionary processes in invaded systems has remained a "black box" for many marine communities.
This special issue focuses on current research advances in the evolutionary biology of marine invasions. The papers presented herein enhance our understanding of the mechanisms of invasion, local adaptation processes, and the interactions of introduced species with native populations in marine environments. The papers in this special issue represent solicited contributions from marine invasion scientists who took part in an inaugural conference called Marine Evolution 2018 and present research at the forefront of this emerging evolutionary field.

| CONTENT OF THE S PECIAL ISSUE
The papers in this special issue were inspired by Marine Evolution 2018, an international conference on evolutionary biology in the marine realm. Pérez-Portela, and Jamie Hudson. Many of the researchers above have contributed papers for this special issue. Finally, keynote speakers gave talks at the start of each day, and one of these keynote speakers, Frederique Viard, is also a contributing author to this special issue.
These papers represent diverse perspectives on the emerging field of evolutionary biology in marine invasions. Early research on marine invasions, and invasion biology more broadly, focused on the significant impacts of non-native organisms on the ecology of an invaded region (Elton, 1958;Richardson, 2011). More recently, researchers have come to understand that evolutionary change may play a key role both in facilitating species invasions and in mediating the response of the native community to new invaders (Lee & Gelembiuk, 2008;Suarez & Tsutsui, 2008). Similarly, just as invasions have become a natural model for understanding how ecological communities function (Blackburn, 2008), they are attracting more research attention as natural experiments in rapid evolution-particularly relevant in this era of rapidly changing climate (Moran & Alexander, 2014). Evolutionary changes at the population level as the result of marine invasions may then influence the larger community of organisms (both native and non-native) in the invaded region and even potentially have ecosystem-level effects, especially for those organisms that play a foundational role (e.g., seaweeds). Papers in this special issue can be broadly classified into a few major avenues of research, which we will introduce in turn: the evolutionary history of invasive populations, postinvasion reproductive changes, and the role of evolution in parasite introductions. The authors found that the species' current genetic makeup has been shaped by a complex network of both ancestral and historical divergence and admixture. An ancestral split occurred between native English Channel and deep-water Sweden populations, with secondary contact between these populations resulting in a distinct native shallow-water Sweden lineage. The introduced northwest Atlantic population, in turn, appears to be the result of admixture between the native English Channel and shallow-Sweden lineages. Their work highlights the important role that divergence and admixture, both ancestral and contemporary, may play in the success of introduced marine species.

| Evolutionary history of invasive populations
The contribution by Simon et al. (2019) advances understanding of the evolutionary mechanisms behind anthropogenic hybridization. The authors studied hybridization between native species and species introduced by shipping. They detected patterns of hybridization in "dock mussels": the blue mussel Mytilus edulis and the Mediterranean mussel M. galloprovincialis. They found that these "dock mussels" formed spatially limited hybrid zones with native mussel species at port entrances.
The observed homogeneous admixture patterns were restricted to large ports, suggesting early-stage adaptation and habitat choice combined with limited gene flow, rather than migration selection.

| Postinvasion reproductive changes
Species introductions may also have a strong impact on the reproductive biology of an invasive species. Reproductive traits may be the target of postinvasion adaptation to novel environments, or a species' reproductive strategy may influence its spread in invaded landscapes. Three papers in this special issue examined the influence of reproduction on invasion from an evolutionary context. Green, Havenhand, and Kvarnemo (2019) investigated postinvasion local adaptation to salinity gradients on sperm motility and viability in a highly invasive fish species in Europe. They sought to determine why invasive round goby Neogobius melanostomus are absent from fully marine waters even though adults appeared tolerant to these higher salinities. The authors tested whether the fish's absence was due to limitations on sperm function at higher salinities, whether local adaptation to higher or lower salinity waters would differentially affect sperm motility, and whether time since introduction played a role. They found that sperm veloc-  where host and parasite are coevolved: The host is native, but the parasite is invasive (short-term coevolution); and the parasite is absent (hosts are naive). This study draws on ecological and metaanalytical data to conclude that parasite prevalence is far higher in hosts where the parasite has invaded versus hosts in the parasite's native range. The authors further tested this relationship with experimental infections, finding that naive hosts were more susceptible to infection than were hosts from the parasite's native (coevolved) range. Together, these results suggest that hosts have evolved over time to resist parasitism and that parasite invasion may have disproportionate effects on previously naive host populations. This study highlights the potential for cascading effects on local ecosystems, as species ranges shift and parasites are introduced into host populations that lack an evolutionary relationship with them.

| CON CLUS I ON S AND FUTURE DIREC TIONS
The papers in this special issue demonstrate the value of investigating marine invasions from an evolutionary perspective and highlight recent technological advances that are key to resolving the uncertainty that often surrounds species invasions. Several papers in this special issue underscore the growing ability of highthroughput sequencing to elucidate evolutionary dynamics in species invasions (Sherman et al., 2016;Viard, David, & Darling, 2016).
While the question of invasion history and source identification has long been an area of active research, the low resolution of traditional molecular tools has hampered our ability to detect subtle differentiation (Estoup & Guillemaud, 2010). This has been a particular issue for marine invasive species, which are often characterized by dynamics such as high dispersal, recent divergence, and complex evolutionary histories that make it difficult to disentangle divergence and admixture at multiple timescales (Darling & Carlton, 2018;Geller et al., 2010). A strong understanding of the evolutionary backgrounds of species invasions, facilitated by high-throughput sequencing, permits the testing of a number of hypotheses regarding the spread and success of marine invasions.
In some systems, admixture (both ancient and recent) may create populations with a rich evolutionary substrate upon which selection pressures in novel environments can act (Keller & Taylor, 2010;Kolbe et al., 2004;Krehenwinkel, Rödder, & Tautz, 2015).
In other cases, successful invaders may be genetically depauperate exemplars of the "genetic paradox of invasion," prompting an examination of the factors that may promote success in the absence of high diversity (Roman & Darling, 2007). As sequencing technologies and analytical approaches improve, we expect to see great improvements in our understanding of the evolutionary pasts-and futures-of marine invasions. A critical component of success in a novel environment is the ability to reproduce successfully, and papers in this special issue also address the importance of selection on reproductive biology.
While selection on reproductive parameters is a major fixture of fundamental evolutionary research, thus far it has not been examined as extensively in marine invasions (Barrett et al. 2008;Manier et al., 2013). As this field of research expands, particularly using careful, well-controlled physiological experimental designs, we anticipate a wealth of insights into this key stage in the establishment of introduced marine species. Prior work examining the "genetic paradox" in marine invasions has noted the key role that asexual reproduction may play in facilitating the success of highly bottlenecked populations (Roman & Darling, 2007;Gutekunst et al., 2018;North, Pennanen, Ovaskainen, & Laine, 2011). This is especially pertinent to organisms with complex life cycles, notably many species of macroalgae, where these complex life cycles may strongly influence their successful establishment and spread in novel environments (Krueger-Hadfield et al., 2016). Adopting an analytical framework that explicitly incorporates a species' reproductive system will greatly improve our understanding of the evolutionary dynamics at play in marine invasions of macroalgae and other species with multiple reproductive options.
Finally, papers in this special issue highlight the importance of evolutionary dynamics in the introduction of marine parasites. While most studies focus on introductions of easily observed, free-living marine species, the invasion of parasites to systems may be cryptic until they reach high levels of host impact (Lymbery, Morine, Kanani, Beatty, & Morgan, 2014). Host-parasite coevolution represents a canonically powerful selection dynamic, and selection is likely to play a substantial role in the dynamics of introduced parasites and their hosts (Hamilton, Axelrod, & Tanese, 1990;Miller & Vincent, 2008;Wendling, Wegner, & Wendling, 2015). While all introduced species run the risk of founder effects, this may be particularly acute for parasites, which must pass through complex, multi-host life cycles to establish in a new region. Successful parasites may have to adapt to new hosts to complete their life cycles in a novel region, with potential evolutionary pressures on both parasite and host (Goedknegt et al., 2016). The impact of parasite introductions may be mediated by the evolutionary history of both parasite and host, with potentially extreme effects on native hosts, which may have no evolved defenses against a novel parasite (Peeler, Oidtmann, Midtlyng, Miossec, & Gozlan, 2011). Our current understanding of the impacts of marine parasites is hampered considerably by a dearth of knowledge of native parasite populations. We suggest that a more complete characterization of marine parasite communities will aid in identifying and studying future parasite introductions.
This special issue presents a range of studies speaking to emerging areas of research on the evolutionary biology of marine invasions. Evolution plays a key role in species survival and persistence in new or changing marine environments. Studies of rapid evolution in marine invasions can thus provide fundamental insights into the speed and nature of rapid adaptive change in the ocean, improving our understanding of how marine species more broadly can adapt to changing seas. Moreover, marine invasions can help us generally understand evolutionary processes in real time since introduced populations can serve as natural experiments in evolution, as non-native species spread and adapt to novel environments. On an applied level, invasion studies can also inform our understanding of the evolutionary traits that facilitate introduction and establishment, improving our ability to predict and prevent future introductions.
We propose that an evolutionary perspective should be integral to marine invasion studies and that such a perspective will benefit both fundamental evolutionary biology and the prediction and management of marine invasions.

ACK N OWLED G EM ENTS
We thank the organizers of Marine Evolution 2018 for bringing together a dynamic group of researchers working in all aspects of marine evolutionary biology and for facilitating the discussion of evolution in marine invasion. We also thank Evolutionary Applications for providing an avenue to share the results of this meeting more broadly and hope it will encourage continued research and discussion of this topic.