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Abstract The α-carbonic anhydrase (αCA) gene family encodes an abundant and ancient metalloenzyme present in all animals. Found in both eukaryotes and prokaryotes, members of this gene family play vital roles in ionic regulation, acid-base regulation, and respiration. However, little is known regarding the evolutionary history and patterns of molecular evolution of this gene family in the phylum Arthropoda, especially in relation to chordates. Through phylogenetic reconstruction and subcellular localization prediction, we discovered that arthropod αCA genes could be classified into three clades based on phylogenetic topology, as has been found in chordate αCA. Among the three distinct arthropod αCA clades, Clade III, enriched in predicted extracellular and cell membrane-bound subcellular localization, exhibited the highest rates of evolution and greatest number of homologs. Intriguingly, we found distinct patterns of gene family expansions and contractions between arthropods and chordates through gene tree-species tree reconciliation. Lastly, we found that αCA12, a member of Clade III αCA, showed signatures of positive selection (based on dN/dS) in two sibling species within the copepod Eurytemora affinis species complex (E. carolleeae and E. gulfia), compared to the general arthropod αCA background. In these populations, this particular paralog had previously shown contemporary signatures of selection during invasions into novel salinities. Overall, our results indicate that the αCA gene family shows signatures of selection both on macroevolutionary time scales across phyla, as well as between closely related sibling species within Arthropoda. 

Rates of biological invasions are accelerating throughout the world. However, our understanding of the evolutionary mechanisms that promote invasive success remains incomplete. Genome architecture can affect mechanisms of rapid and parallel evolution during invasions. In aquatic habitats, many invaders are crossing biogeographical boundaries from saline to freshwater habitats. The copepod Eurytemora affinis species complex provides a valuable model system for analyzing evolutionary mechanisms underlying these invasions, with populations that have recently invaded freshwater habitats multiple times independently from saline sources. Surprisingly, parallel selection favors the same alleles repeatedly during these invasions, even across clades with differing chromosome number, indicating that salinity adaptation proceeds in a predictable manner. Genome architecture appears to have profound impacts on the response to selection in these populations, with chromosome number likely impacting the relative importance of standing genetic variation versus positive epistasis in promoting parallel evolution. More research is needed to fully explore the role of genome architecture in impacting population responses to selection, especially during habitat invasions. 

Under radical environmental change, populations may need to adapt quickly to avoid substantial declines in abundance and threats to their persistence. The outcome of this race between evolution and demography depends on the genetic architecture of adaptation, which determines how fast evolution can proceed. In particular, adaptation may require coordinated evolution at multiple loci (e.g., cooperating ion transporters for ion uptake), with single-locus changes being deleterious. Such selection on coadapted genes leads to a fitness landscape with a valley, which can in turn favor the evolution of structural variants that link beneficial alleles at different loci. Here, we investigate how epistasis and recombination jointly affect population dynamics under such a fitness valley. We assume that adaptation occurs from standing genetic variation and model the eco-evolutionary dynamics deterministically. We show that recombination has strong impacts on population decline and recovery in this context. Higher recombination rates cause evolutionary trajectories to be pulled toward unfit states, leading to prolonged evolutionary plateaus, during which the population can decline precipitously. In highly detrimental cases where coadapted mutations are located on different chromosomes, chromosomal fusions that are preexisting at low frequency can lead to faster population recovery by allowing the genetic system to escape the attraction to unfit intermediate states. Our results provide insights into eco-evolutionary dynamics in systems where chromosome number varies drastically among sibling species, such as the copepod Eurytemora affinis species complex, and offer new perspectives on the impacts of genome architecture on population dynamics in stressful environments. 

Climate change is threatening aquatic populations with rapid changes in habitat salinity and temperature. Locally adapted alleles along environmental gradients, along with low but sufficient gene flow, could provide crucial genetic variation to adapt to future climate change and rescue populations from extinction. Thus, we explored whether planktonic populations exhibit genomic signatures of selection and gene flow across salinity and temperature gradients in the Baltic Sea and North Sea region. LocationBaltic Sea, North Sea region. MethodsWe performed whole‐genome sequencing of 11 populations of the copepodEurytemora affinisproper along salinity and temperature gradients. We determined signatures of population structure, admixture, and natural selection by analysing single nucleotide polymorphism (SNP) frequencies across populations using TreeMix, PoPoolation2, poolfstat, and BayPass. ResultsWe found significant population genomic signatures of selection associated with salinity and temperature gradients using BayPass X^TX and environmental association tests, consistent with local adaptation. Several ion transport functional categories (GO terms) were significantly associated with the salinity gradient across all populations, whereas only one GO term, ‘prostaglandin biosynthetic process’, was significantly associated with the temperature gradient in the North Sea region. We found clear population structure with PoPoolation2 and TreeMix. We also found signals of admixture between populations with poolfstat and TreeMix, consistent with the presence of gene flow. Site‐frequency spectra (SFS) of candidate SNPs tested against simulated SFS distributions revealed an excess of intermediate frequency alleles within a few populations. Main ConclusionsThe interplay between local adaptation and gene flow had not been fully explored in passive holoplankton dispersers. Many of the same ion transporter genes showed signatures of selection as in our prior studies, but in this case across a metapopulation ofE. affinisspanning a broad geographic range. The presence of locally adapted alleles along with gene flow across environmental gradients could provide genetic substrate for natural selection, enabling populations to adapt to future climate change. 

Abstract Chromosomal fusions are hypothesized to facilitate evolutionary adaptation, but empirical evidence has been scarce. Here, we analyze chromosome-level genome sequences of three sibling species within the copepodEurytemora affinisspecies complex, known for its remarkable ability to rapidly colonize new habitats. Genomes of this species complex show expansions of ion transport-related gene families, likely related to adaptation to various environmental salinities. Among three genetically distinct sibling species, we discover notable patterns of chromosomal evolution, with chromosomal fusions observed in two different sibling species. As a result of these chromosomal fusions, functionally linked ion transport-related genes located near the telomeres become joined near the newly formed centromeres, where recombination is low. Notably, for the highly invasiveE. carolleeaeand to a lesser extent forE. gulfia, the ancient chromosomal fusion sites, especially the centromeres, are significantly enriched with contemporary signatures of selection between saline and freshwater populations. This study uncovers intriguing patterns of genome architecture evolution with potentially important implications for mechanisms of adaptive evolution in response to rapid environmental change. 

Abstract Copepods are among the most abundant organisms on the planet and play critical functions in aquatic ecosystems. Among copepods, populations of the Eurytemora affinis species complex are numerically dominant in many coastal habitats and serve as food sources for major fisheries. Intriguingly, certain populations possess the unusual capacity to invade novel salinities on rapid time scales. Despite their ecological importance, high-quality genomic resources have been absent for calanoid copepods, limiting our ability to comprehensively dissect the genome architecture underlying the highly invasive and adaptive capacity of certain populations. Here, we present the first chromosome-level genome of a calanoid copepod, from the Atlantic clade (Eurytemora carolleeae) of the E. affinis species complex. This genome was assembled using high-coverage PacBio long-read and Hi-C sequences of an inbred line, generated through 30 generations of full-sib mating. This genome, consisting of 529.3 Mb (contig N50 = 4.2 Mb, scaffold N50 = 140.6 Mb), was anchored onto four chromosomes. Genome annotation predicted 20,262 protein-coding genes, of which ion transport-related gene families were substantially expanded based on comparative analyses of 12 additional arthropod genomes. Also, we found genome-wide signatures of historical gene body methylation of the ion transport-related genes and the significant clustering of these genes on each chromosome. This genome represents one of the most contiguous copepod genomes to date and is among the highest quality marine invertebrate genomes. As such, this genome provides an invaluable resource to help yield fundamental insights into the ability of this copepod to adapt to rapidly changing environments. 

With climate change, habitat salinity is shifting rapidly throughout the globe. In addition, many destructive freshwater invaders are recent immigrants from saline habitats. Recently, populations of the copepod Eurytemora affinis species complex have invaded freshwater habitats multiple times independently from saline estuaries on three continents. This review discusses features of this species complex that could enhance their evolutionary potential during rapid environmental change. Remarkably, across independent freshwater invasions, natural selection has repeatedly favored the same alleles far more than expected. This high degree of parallelism is surprising, given the expectation of nonparallel evolution for polygenic adaptation. Factors such as population structure and the genome architecture underlying critical traits under selection might help drive rapid adaptation and parallel evolution. Given the preponderance of saline-to-freshwater invasions and climate-induced salinity change, the principles found here could provide invaluable insights into mechanisms operating in other systems and the potential for adaptation in a changing planet. 

While many freshwater invaders originate from saline habitats, the physiological mechanisms involved are poorly understood. We investigated the evolution of ion transporter Na+/K+-ATPase (NKA) protein expression between ancestral saline and freshwater invading populations of the copepod Eurytemora carolleae (Atlantic clade of the E. affinis complex). We compared in situ NKA expression between populations under common-garden conditions at three salinities in the maxillary glands. We found the evolution of reduced NKA expression in the freshwater population under freshwater conditions and reduced plasticity (canalization) across salinities, relative to the saline population. Our results support the hypothesis that maxillary glands are involved in ion reabsorption from excretory fluids at low-salinity conditions in the saline population. However, mechanisms of freshwater adaptation, such as increased ion uptake from the environment, might reduce the need for ion reabsorption in the freshwater population. These patterns of ion transporter expression contribute insights into the evolution of ionic regulation during habitat change. 

Life in fresh water is osmotically and energetically challenging for living organisms, requiring increases in ion uptake from dilute environments. However, mechanisms of ion uptake from freshwater environments are still poorly understood and controversial, especially in arthropods, for which several hypothetical models have been proposed based on incomplete data. One compelling model involves the proton pump V-type H + ATPase (VHA), which energizes the apical membrane, enabling the uptake of Na + (and other cations) via an unknown Na + transporter (referred to as the “Wieczorek Exchanger” in insects). What evidence exists for this model of ion uptake and what is this mystery exchanger or channel that cooperates with VHA? We present results from studies that explore this question in crustaceans, insects, and teleost fish. We argue that the Na + /H + antiporter (NHA) is a likely candidate for the Wieczorek Exchanger in many crustaceans and insects; although, there is no evidence that this is the case for fish. NHA was discovered relatively recently in animals and its functions have not been well characterized. Teleost fish exhibit redundancy of Na + uptake pathways at the gill level, performed by different ion transporter paralogs in diverse cell types, apparently enabling tolerance of low environmental salinity and various pH levels. We argue that much more research is needed on overall mechanisms of ion uptake from freshwater habitats, especially on NHA and other potential Wieczorek Exchangers. Such insights gained would contribute greatly to our general understanding of ionic regulation in diverse species across habitats.