LEE LAB Department of Integrative Biology University of Wisconsin - Madison  430 Lincoln Drive, Birge 420 University of Wisconsin Madison, WI 53706 Office:  (608) 262-2675 Lab:  (608) 262-9225 Email: carollee@wisc.edu

Evolutionary Genetics of Invasive Populations

As invasive species represent the rare victors during habitat transitions, they provide invaluable models for understanding mechanisms of niche evolution and responses to environmental change. Thus, one branch of research in my laboratory explores patterns and mechanisms of rapid evolution during contemporary invasions into novel habitats. Of the large number of species that are introduced into new habitats, few are successful as invaders (Williamson and Fitter 1996). What allows some species to invade, when most cannot? There is increasing recognition that response to selection can be important (Lee 2002). As successful invaders are aberrations from the norm, their habitat shifts could yield insights into fundamental constraints on evolvability and adaptation (Lee & Gelembiuk 2008).

A comparative and integrative approach offers the power to infer characteristics of invasive populations.  Thus, we are examining patterns and mechanisms of phenotypic evolution (1) between ancestral source and invading populations, (2) among multiple independent invasions, and (3) between invasive and noninvasive populations within species.  Direct comparisons of source and invading populations reveal evolutionary adaptations that are associated with habitat transitions (Lee et al. 2003; Lee et al. 2007; Lee et al., 2011; Posavi et al. 2020; Stern & Lee 2020).  Analysis of multiple independent invasions offers insights into repeatability of evolutionary pathways (Lee 1999; Stern & Lee 2020).  Finally, comparing invasive and noninvasive populations uncovers properties that are exclusive of successful invaders (Lee et al. 2013).  In addition, links between colonization and speciation (Mayr 1942) have led to the study of (4) patterns of reproductive isolation and incipient speciation following geographic separation (Lee 2000; Lee & Frost 2002). Research in my laboratory focuses on some of the most pervasive invaders in aquatic ecosystems, such as populations of the copepod Eurytemora affinis  species complex and zebra and quagga mussels (Dreissena polymorpha and D. bugensis).

Rapid Physiological Evolution during Independent Invasions

Habitat invasions, and geographic range shifts in general, present important forces for adaptation and speciation, but had not been incorporated into the Evolutionary Synthesis. A relatively marginal figure during that time period, C. H. Waddington, did recognize that habitat shifts could serve as important mechanisms for rapid adaptation (by exposing novel phenotypes to selection) (Waddington 1965). Curiously, many species that are currently dominating freshwater habitats are recent invaders from saline environments (Casties et al. 2016; Lee & Bell 1999). For example, the vast majority of recent invaders into the Great Lakes have originated from the Black and Caspian Sea region (Casties et al. 2016; Lee & Bell 1999). As most animal phyla have evolved in the sea, fresh water imposes physiological challenges for most taxa (Hutchinson 1957; Lee & Bell 1999).

Eurytemora affinis species complex

Research in my lab is currently focusing on linking genomic analyses with physiological function associated with adaptation to novel environments. We are exploring the physiological and genomic targets of selection during independent freshwater invasions. Examining the repeatability of mechanisms underlying freshwater adaptation could reveal the extent to which these evolutionary pathways are labile or constrained.  

The copepod Eurytemora affinis species complex provides an exceptional model for exploring mechanisms of niche evolution.  Within the past century, populations from this species complex have invaded freshwater habitats from saline sources throughout the Northern Hemisphere.  Freshwater invasions have occurred multiple times independently from genetically distinct sources (Lee 1999) (Fig. 1), offering replicated natural experiments in the wild. The short generation time (20 d) offers a system that enables laboratory selection experiments  and genetic association studies to identify the selective forces and link genotype with phenotype. The relatively small genome (500 Mb) and availability of high quality genomic resources (PacBio full genomes) offers the ability to uncover the genetic loci under selection during habitat shifts.

Research in my laboratory has yielded several key results regarding evolutionary shifts during habitat invasions.  For example, common-garden experiments have revealed evolutionary shifts in salinity tolerance and life history traits during freshwater invasions (Lee et al. 2003; Lee et al. 2007).  Freshwater populations showed increases in freshwater tolerance and reduced saltwater tolerance relative to their saline ancestors (Lee et al. 2003; Lee et al. 2007), as well as evolutionary shifts in ionic regulation (Lee et al. 2011; Lee et al. 2012).  These shifts appear to have arisen through selection on standing genetic variation within saline source populations (Lee et al. 2003; Stern & Lee 2020), rather than through acclimation (Lee and Petersen 2003). Genome-wide gene expression analyses have revealed evolutionary shifts in gene expression between ancestral saline and freshwater derived populations (Posavi et al. 2020). Moreover, we found striking patterns of parallel selection across independent invasions, with an enrichment of ion transporter paralogs under selection (Stern & Lee 2020; Stern et al. In Revision) (Fig. 2). Functional assays of some of the ion transporters under selection have revealed evolutionary shifts in enzyme activity that are consistent with evolutionary shifts in gene expression (Lee et al. 2011). We have performed in situ immunolocalization of the ion tranporter paralogs under selection and identified the cells, tissues, and organs that are responsible for physiological transformations during habitat invasions (Johnson et al. 2014; Gerber et al. 2016) to enhance our understanding of functional evolution. 

The selection regime of the source habitat might have profound effects on the propensity to invade (Winkler et al. 2008; Lee & Gelembiuk 2008). We hypothesized that environmental stress and/or fluctuating conditions in the native range could impose selection regimes that lead to the evolution of invasive populations, through the action of balancing selection (Lee & Gelembiuk 2008).  Additionally, we uncovered a plausible mechanism that would promote the maintenance of genetic variation under a fluctuating selection regime (Posavi et al. 2014). Moreover, we found that the very same alleles (SNPs) that show parallel signatures of selection in freshwater invading populations also show signatures of balancing selection in their native range populations (Stern & Lee 2020), consistent with our hypothesis. Most notably, some clades have given rise to invasive populations, while others have not (Lee 1999; Lee 2000) (Fig. 1). The fact that noninvasive clades tend to occur in more constant habitats might account for their limited range expansions. Populations from invasive and noninvasive clades show striking differences in their physiological response to fresh water, with greater low-salinity tolerance and starvation resistance in the invasive clade (Lee et al. 2013). We are continuing to explore the role of balancing selection in the native range and the effects of synergistic epistasis among the candidate alleles in promoting rapid and parallel adaptation during habitat shifts. 

 

The long-term research interests of my laboratory focus on evolutionary dynamics at the interface between habitat boundaries, and factors that allow shifts in habitat type.  Results from our work not only have broad implications for biological invasions, but also for global change, habitat restoration and acclimatization, and macroevolutionary processes, such as the colonization of land.  The approaches I have outlined above, integrating phylogenetics, physiology, biochemistry, and genomics can be used to address diverse questions regarding physiological and biochemical responses to environmental clines (such as gradients in temperature, oxygen, irradiation, and nutrients). 

References

Hutchinson, G. E. 1957. A Treatise on Limnology. John Wiley & Sons, Inc., New York.

Casties et al. 2016. Importance of geographic origin for invasion success: A case study of the North and Baltic Seas versus the Great Lakes–St. Lawrence River region. Ecology and Evolution. 6:8318–8329.

Gerber L, CE Lee, E Grousset, E Blondeau-Bidet, NB Boucheker, C Lorin-Nebel, M Charmantier-Daures, G Charmantier. 2016. The Legs Have It: Localizing and quantifying expression of ion transporters V-Type H⁺ ATPase and Na⁺/K⁺-ATPase in the swimming legs of the freshwater invading copepod Eurytemora affinis. Physiological and Biochemical Zoology. 89:233-250.

Johnson KE, L Perreau, G Charmantier, M Charmantier-Daures, CE Lee. 2014. Without Gills: Exploring the localization of osmoregulatory function in the copepod Eurytemora affinis. Physiological and Biochemical Zoology. 87:310-324.

Lee, CE. 1999. Rapid and repeated invasions of fresh water by the saltwater copepod Eurytemora affinis. Evolution. 53:1423-1434.

Lee, CE. 2000. Global phylogeography of a cryptic copepod species complex and reproductive isolation between genetically proximate "populations". Evolution. 54:2014-2027.

Lee, CE. 2002. Evolutionary genetics of invasive species. Trends in Ecology and Evolution. 17:386-391.

Lee, CE, MA Bell. 1999. Causes and consequences of recent freshwater invasions by saltwater animals. Trends in Ecology and Evolution. 14:284-288.

Lee, CE, BW Frost. 2002. Morphological Stasis in the Eurytemora affinis species complex (Copepoda: Temoridae). Hydrobiologia. 480:111-128.

Lee, CE, GW Gelembiuk. 2008. Evolutionary Origins of invasive populations. Evolutionary Applications. 1:427-448.

Lee CE, M Kiergaard, BD Eads, GW Gelembiuk, M Posavi.  2011.  Pumping ions: Rapid parallel evolution of ionic regulation following habitat invasions. Evolution. 65:2229-2244.

Lee CE, W Moss, N Olson, KF Chau, YM Chang, K Johnson.  2013. Feasting in fresh water: Impacts of food concentration on freshwater tolerance and the evolution of food x salinity response during the expansion from saline into freshwater habitats. Evolutionary Applications. 6:673-689.

Lee, CE, CH Petersen. 2003. Effects of developmental acclimation on adult salinity tolerance in the freshwater-invading copepod Eurytemora affinis. Physiological and Biochemical Zoology. 76:296-301.

Lee CE, M Posavi, G Charmantier. 2012. Rapid evolution of body fluid regulation following independent invasions into freshwater habitats. Journal of Evolutionary Biology. 25:625-633.

Lee, CE, JL Remfert, YM Chang. 2007. Response to selection and evolvability of invasive populations. Genetica. 129:179-192.

Lee, CE, JL Remfert, GW Gelembiuk. 2003. Evolution of physiological tolerance and performance during freshwater invasions. Int. Comp. Biol. 43:439-449.

Posavi M, GW Gelembiuk, B Larget, CE Lee. 2014. Testing for beneficial reversal of dominance during salinity shifts in the invasive copepod Eurytemora affinis, and implications for the maintenance of genetic variation. Evolution. 68:3166-3183.

Posavi M, D Gulisija, JC Silva, CE Lee. 2020. Rapid evolution of genome-wide expression and plasticity during saline to freshwater invasions by a copepod. Molecular Ecology. 29:4835-4856. DOI: 10.1111/mec.15681

Stern DB, CE Lee. 2020. Evolutionary origins of genomic adaptations in an invasive copepod. Nature Ecology and Evolution. 4:1084-1094.  https://doi.org/10.1038/s41559-020-1201-y Supplementary Tables

Mayr, E. 1942. Systematics and the Origin of Species, Columbia University Press, New York.

Waddington, C. H. 1965. Introduction to the Symposium. Pp. 1-6 in H. G. Baker, and G. L. Stebbins, eds. The Genetics of Colonizing Species. Academic Press, New York.

Williamson, M, A Fitter. 1996. The varying success of invaders. Ecology. 77:1661-1666.

Winkler, G, J Dodson, CE Lee. 2008. Heterogeneity within the native range:  Population genetic analyses of sympatric invasive and noninvasive populations of the freshwater invading copepod Eurytemora affinis. Molecular Ecology. 17:415-430.