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1. The Legs Have It: In Situ Expression of Ion Transporters V-Type H ⁺ -ATPase and Na ⁺ /K ⁺ -ATPase in the Osmoregulatory Leg Organs of the Invading Copepod Eurytemora affinis

   https://doi.org/10.1086/686323  

   Gerber, Lucie; Lee, Carol Eunmi; Grousset, Evelyse; Blondeau-Bidet, Eva; Boucheker, Nesrine Boudour; Lorin-Nebel, Catherine; Charmantier-Daures, Mireille; Charmantier, Guy (May 2016, Physiological and Biochemical Zoology)

   null (Ed.)

   The copepod Eurytemora affinis has an unusually broad salinity range, as some populations have recently invaded freshwater habitats independently from their ancestral saline habitats. Prior studies have shown evolutionary shifts in ion transporter activity during freshwater invasions and localization of ion transporters in newly discovered "Crusalis organs" in the swimming legs. The goals of this study were to localize and quantify expression of ion transport enzymes V-type H(+)-ATPase (VHA) and Na(+)/K(+)-ATPase (NKA) in the swimming legs of E. affinis and determine the degree of involvement of each leg in ionic regulation. We confirmed the presence of two distinct types of ionocytes in the Crusalis organs. Both cell types expressed VHA and NKA, and in the freshwater population the location of VHA and NKA in ionocytes was, respectively, apical and basal. Quantification of in situ expression of NKA and VHA established the predominance of swimming leg pairs 3 and 4 in ion transport in both saline and freshwater populations. Increases in VHA expression in swimming legs 3 and 4 of the freshwater population (in fresh water) relative to the saline population (at 15 PSU) arose from an increase in the abundance of VHA per cell rather than an increase in the number of ionocytes. This result suggests a simple mechanism for increasing ion uptake in fresh water. In contrast, the decline in NKA expression in the freshwater population arose from a decrease in ionocyte area in legs 4, likely resulting from decreases in number or size of ionocytes containing NKA. Such results provide insights into mechanisms of ionic regulation for this species, with added insights into evolutionary mechanisms underlying physiological adaptation during habitat invasions. 

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2. Response to selection and evolvability of invasive populations

   https://doi.org/10.1007/s10709-006-9013-9  

   Lee, Carol Eunmi; Remfert, Jane Louise; Chang, Yu-Mei (February 2007, Genetica)

   While natural selection might in some cases facilitate invasions into novel habitats, few direct measurements of selection response exist for invasive populations. This study examined selection response to changes in salinity using the copepod Eurytemora affinis. This copepod has invaded fresh water from saline habitats multiple times independently throughout the Northern Hemisphere. Selection response to a constant intermediate salinity (5 PSU) was measured in the laboratory for saline source and freshwater invading populations from the St. Lawrence drainage (North America). These populations were reared under three conditions: (1) native salinities (0 or 15 PSU) for at least two generations, (2) 5 PSU for two generations, and (3) 5 PSU for six generations. Full-sib clutches taken from populations reared under these three conditions were split across four salinities (0, 5, 15, and 25 PSU) to determine reaction norms for survival and development time. Contrasts in survival and development time across the three rearing conditions were treated as the selection response. Selection at 5 PSU resulted in a significant decline in freshwater (0 PSU) tolerance for both the saline and freshwater populations. Yet, evolutionary differences in freshwater tolerance persisted between the saline and freshwater populations. The saline and freshwater populations converged in their high-salinity (25 PSU) tolerance, with an increase in the freshwater population and decline in the saline population. Development time did not shift greatly in response to selection at 5 PSU. For all three rearing conditions, the freshwater population exhibited retarded larval development and accelerated juvenile development relative to the saline population. Results from this study indicate that both the saline and freshwater populations exhibit significant responses to selection for a fitness-related trait critical for invasions into a novel habitat. 

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3. Rapid evolution of body fluid regulation following independent invasions into freshwater habitats: Evolution of body fluid regulation

   https://doi.org/10.1111/j.1420-9101.2012.02459.x  

   LEE, CAROL EUNMI; POSAVI, MARIJAN; CHARMANTIER, GUY (April 2012, Journal of Evolutionary Biology)

   Colonizations from marine to freshwater environments constitute among the most dramatic evolutionary transitions in the history of life. Colonizing dilute environments poses great challenges for acquiring essential ions against steep concentration gradients. This study explored the evolution of body fluid regulation following freshwater invasions by the copepod Eurytemora affinis. The goals of this study were to determine (1) whether invasions from saline to freshwater habitats were accompanied by evolutionary shifts in body fluid regulation (hemolymph osmolality) and (2) whether parallel shifts occurred during independent invasions. We measured hemolymph osmolality for ancestral saline and freshwater invading populations reared across a range of common-garden salinities (0.2-25 PSU). Our results revealed the evolution of increased hemolymph osmolality (by 16-31%) at lower salinities in freshwater populations of E. affinis relative to their saline ancestors. Moreover, we observed the same evolutionary shifts across two independent freshwater invasions. Such increases in hemolymph osmolality are consistent with evidence of increased ion uptake in freshwater populations at low salinity, found in a previous study, and are likely to entail increased energetic costs upon invading freshwater habitats. Our findings are consistent with the evolution of increased physiological regulation accompanying transitions into stressful environments. 

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4. Evolution of Physiological Tolerance and Performance During Freshwater Invasions

   https://doi.org/10.1093/icb/43.3.439  

   Lee, Carol Eunmi (July 2003, Integrative and Comparative Biology)

   Invasive species that penetrate habitat boundaries are likely to experience strong selection and rapid evolution. This study documents evolutionary shifts in tolerance and performance following the invasion of fresh water by the predominantly estuarine and salt marsh copepod Eurytemora affinis. Common-garden experiments were performed on freshwater-invading (Lake Michigan) and ancestral saline (St. Lawrence marsh) populations to measure shifts in adult survival (at 0, 5, and 25 PSU), and survival during development and development time (both using full-sib clutches split across 0, 5, 15, and 25 PSU). Results showed clear evidence of heritable shifts in tolerance and performance associated with freshwater invasions. The freshwater population exhibited a gain in low-salinity tolerance and a reduction in high-salinity tolerance relative to the saline population, suggesting tradeoffs. These tradeoffs were supported by negative genetic correlations between survival at fresh (0 PSU) versus higher salinities. Mortality in response to salinity occurred primarily before metamorphosis, suggesting that selection in response to salinity had acted primarily on the early life-history stages. The freshwater population exhibited curious patterns of life-history evolution across salinities, relative to the saline population, of retarded development to metamorphosis but accelerated development from metamorphosis to adulthood. This pattern might reflect tradeoffs between development rate and survival in fresh water at the early life-history stages, but some other selective force acting on later life-history stages. Significant effects of clutch (genotype) and clutch-by-salinity interaction (G × E) on survival and development time in both populations indicated ample genetic variation as substrate for natural selection. Variation for high-salinity tolerance was present in the freshwater population despite negative genetic correlations between high- and low-salinity tolerance. Results implicate the importance of natural selection and document the evolution of reaction norms during freshwater invasions. 

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5. Feasting in fresh water: impacts of food concentration on freshwater tolerance and the evolution of food × salinity response during the expansion from saline into fresh water habitats

   https://doi.org/10.1111/eva.12054  

   Lee, Carol Eunmi; Moss, Wynne E.; Olson, Nora; Chau, Kevin Fongching; Chang, Yu‐Mei; Johnson, Kelsey E. (June 2013, Evolutionary Applications)

   Saline to freshwater invasions have become increasingly common in recent years. A key hypothesis is that rates of freshwater invasions have been amplified in recent years by increased food concentration, yet this hypothesis has remained unexplored. We examined whether elevated food concentration could enhance freshwater tolerance, and whether this effect evolves following saline to freshwater invasions. We examined physiological response to salinity and food concentration in a 2 × 2 factorial design, using ancestral brackish and freshwater invading populations of the copepod Eurytemora affinis. We found that high food concentration significantly increases low-salinity tolerance. This effect was reduced in the freshwater population, indicating evolution following the freshwater invasion. Thus, ample food could enable freshwater invasions, allowing subsequent evolution of low-salinity tolerance even under food-poor conditions. We also compared effects of food concentration on freshwater survival between two brackish populations from the native range. Impacts of food concentration on freshwater survival differed between the brackish populations, suggesting variation in functional properties affecting their propensity to invade freshwater habitats. The key implication is that high food concentration could profoundly extend range expansions of brackishwater species into freshwater habitats, potentially allowing for condition-specific competition between saline invaders and resident freshwater species. 

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