Freshwater Resident Populations Research Articles

A key evolutionary step determining osmoregulatory ability for freshwater colonisation in early life stage of fish.

Colonisation of freshwater habitats by marine animals is a remarkable evolutionary event that has enriched biodiversity in freshwater ecosystems. The acquisition of the tolerance to hypotonic stress during the early life stages is presumed to be essential for their successful freshwater colonisation, but very little empirical evidence has been obtained to support this idea. This study aimed to comprehend the evolutionary changes of osmoregulatory mechanisms that enhance the larval freshwater tolerance in amphidromous fishes, which typically spend their larval period in marine (ancestral) habitats and the rest of life history stages in freshwater (derived) habitats. We compared the life history patterns and changes in larval survivorship and gene expression depending on salinity among three congeneric marine-originated amphidromous goby species (Gymnogobius), which had been suggested to differ in their larval dependence on freshwater habitats. An otolith microchemical analysis and laboratory-rearing experiment confirmed the presence of freshwater residents only in G. urotaenia and higher larval survivorship of this species in the freshwater condition than the obligate amphidromous G. petschiliensis and G. opperiens. Larval whole-body transcriptome analysis revealed that G. urotaenia from both amphidromous and freshwater-resident populations exhibited the greatest differences in expression levels of several osmoregulatory genes, including aqp3, which is critical for water discharge from their body during early fish development. The present results consistently support the importance of enhanced freshwater tolerance and osmoregulatory plasticity in larval fish to establish freshwater forms, and further identified key candidate genes for larval freshwater adaptation and colonisation in the goby group.

Does the loss of diadromy imply the loss of salinity tolerance? A gene expression study with replicate nondiadromous populations of Galaxias maculatus.

The recurrent colonization of freshwater habitats and subsequent loss of diadromy is a major ecological transition that has been reported in many ancestrally diadromous fishes. Such residency is often accompanied by a loss of tolerance to seawater. The amphidromous Galaxias maculatus has repeatedly colonized freshwater streams with evidence that freshwater-resident populations exhibit stark differences in their tolerance to higher salinities. Here, we used transcriptomics to gain insight into the mechanisms contributing to reduced tolerance to higher salinities in freshwater resident populations. We conducted an acute salinity challenge (0ppt to 23-25 ppt) and measured osmoregulatory ability (muscle water content) over 48 h in three populations: diadromous, saltwater intolerant resident (Toltén), and saltwater tolerant resident (Valdivia). RNA sequencing of the gills identified genes that were differentially expressed in association with the salinity change and associated with the loss of saltwater tolerance in the Toltén population. Key genes associated with saltwater acclimation were characterized in diadromous G. maculatus individuals, some of which were also expressed in the saltwater tolerant resident population (Valdivia). We found that some of these "saltwater acclimation" genes, including the cystic fibrosis transmembrane conductance regulator gene (CFTR), were not significantly upregulated in the saltwater intolerant resident population (Toltén), suggesting a potential mechanism for the loss of tolerance to higher salinities. As the suite of differentially expressed genes in the diadromous-resident comparison differed between freshwater populations, we hypothesize that diadromy loss results in unique evolutionary trajectories due to drift, so the loss of diadromy does not necessarily lead to a loss in upper salinity tolerance.

Genetic variation within and among range-wide populations of three ecotypes of the Japanese grenadier anchovy Coilia nasus with implications to its conservation and management

Studies of range-wide populations can contribute to the comprehension of the relative roles of historical events and contemporary factors that influence genetic variation within and among populations. Japanese grenadier anchovy, Coilia nasus, is a commercially important fish, which widely distributes in the Changjiang River, the coasts of China and Korea, and the Ariake Sea of Japan. This species exhibits three life-history strategies (anadromous, landlocked and freshwater resident forms). Using two fragments of nuclear DNA, genetic variation within and among 18 populations across the rivers and coast of China and Ariake Sea of Japan was examined. Patterns of genetic diversity and divergence among populations varied widely across C. nasus’ range, and indicated the different effects of historical events and anthropogenic factors. Strong genetic divergence between freshwater resident populations and other populations suggested that historical geographical factors greatly influenced the genetic structure of C. nasus. Significant genetic differentiation observed among lakes in lower Changjiang River and Huaihe River might be probably influenced by hydraulic facilities. The population genetic structure among the three ecotypes revealed in the present study indicated an important role for environment variation, and the factors responsible for shaping C. nasus different life history strategies might also impact population structure.

Comparative proteomic analysis of olfactory rosettes in anadromous Coilia nasus and resident Coilia nasus

The Japanese grenadier anchovy ( Coilia nasus ) undergoes upstream migration to spawning annually but can also be observed in freshwater resident populations. It has been hypothesized that anadromous adult C. nasus may utilize olfactory cues to locate spawning grounds. We firstly performed a comparative proteome analysis about olfactory rosettes in two populations to hunt for the proteomic changes. Among 5 408 identified proteins, 1 515 proteins (629 up-regulated and 886 down-regulated) were differentially expressed. Especially, several proteins and pathways associated with olfactory signaling were found to be significantly differential. Compared with resident C. nasus, the expressions of Golf protein and the sodium/calcium exchanger were significantly up-regulated in anadromous C. nasus. The expression of adenylate cyclase and regulator of G-protein signaling (RGS) were decreased. Our findings suggest a decrease in the expression of cGMP-dependent protein kinase (PKG) in anadromous C. nasus compared to resident C. nasus. The expression of Calmodulin (CaM) was increased and CaM-dependent protein kinase II (CaMKII) was decreased. In addition, KEGG pathway enrichment analysis of up-regulated proteins indicated statistically significant difference not only in olfactory transduction but also in the cGMP-PKG signal pathway. Furtherly, we sought out some proteins expressed in the same trend occurring in DEGs (differentially expressed genes) and DEPs (differentially expressed proteins) by doing the integrative analysis of proteome and transcriptome in olfactory rosettes of C. nasus.

Comprehensive assessment of population genetic structure of the overexploited Japanese grenadier anchovy (Coilia nasus): Implications for fisheries management and conservation

Japanese grenadier anchovy, Coilia nasus, is a commercially important fish species in China. Three ecotypes (anadromous, landlocked and freshwater-resident populations) are distributed across its range. Due to anthropogenic activities such as overfishing and habitat deterioration, the stock status of this species has sharply declined. Clarifying population genetic structure and genetic relationships among ecotypes is essential for the conservation and stock management of C. nasus. Using 18 microsatellite loci, the distribution of genetic variation among 18 geographic populations (nine anadromous populations, four landlocked populations, and five freshwater-resident populations) was examined. High levels of genetic diversity were observed in all populations. Significant genetic differentiation among populations was detected and four genetic groups were identified, which might arise from current geographic segregation, different life-history strategy, and historical geographical factors. High assignment accuracies (≥85%) accessed for all populations suggested microsatellite loci can be used as an effective tool for discriminating the origin of individuals. Our study provided valuable information for conservation and sustainable management of C. nasus across its entire distribution range, and demonstrated the utility of microsatellite data to inform conservation units in highly exploited species.

Contemporary factors influencing genetic diversity in the Alaska humpback whitefish Coregonus clupeaformis complex.

Thirteen microsatellite loci were used to address three hypotheses regarding genetic diversity in the humpback whitefish Coregonus clupeaformis complex in Alaska. The test results provided further insight into the factors influencing C. clupeaformis complex population structure and level of genetic variation. First, the microsatellite data did not provide evidence of two spatially distinct Beringian and Eurasian refugial groups as revealed in previous phylogeographic analyses of mitochondrial DNA variation. Rather, the population structure inferred from the microsatellite variation appears to reveal the influence of factors on a more recent time scale, including gene flow among the refugial groups and isolation of some anadromous and freshwater resident populations. Second, anadromous C. clupeaformis complex collections exhibited higher intra-population genetic diversity than freshwater resident collections. This outcome is consistent with previous meta analyses suggesting that freshwater resident populations probably have smaller historical effective population sizes and less conspecific gene flow because the habitat tends to be smaller and supports fewer and smaller populations. Finally, the analysis of contemporary immigration rates was consistent with, but did not provide statistical support for, the hypothesis that gene flow among anadromous C. clupeaformis complex populations along coastal Alaska is influenced by the Alaska Coastal Current. Further studies are needed to evaluate gene flow among coastal Alaska C. clupeaformis complex populations.

Genomic population structure of freshwater-resident and anadromous ide (Leuciscus idus) in north-western Europe.

Climate change experts largely agree that future climate change and associated rises in oceanic water levels over the upcoming decades, will affect marine salinity levels. The subsequent effects on fish communities in estuarine ecosystems however, are less clear. One species that is likely to become increasingly affected by changes in salinity is the ide (Leuciscus idus). The ide is a stenohaline freshwater fish that primarily inhabits rivers, with frequent anadromous behavior when sea salinity does not exceed 15%. Unlike most other anadromous Baltic Sea fish species, the ide has yet to be subjected to large-scale stocking programs, and thus provides an excellent opportunity for studying the natural population structure across the current salinity gradient in the Danish Belts. To explore this, we used Genotyping-by-Sequencing to determine genomic population structure of both freshwater resident and anadromous ide populations in the western Baltic Sea region, and relate the results to the current salinity gradient and the demographic history of ide in the region. The sample sites separate into four clusters, with all anadromous populations in one cluster and the freshwater resident populations in the remaining three. Results demonstrate high level of differentiation between sites hosting freshwater resident populations, but little differentiation among anadromous populations. Thus ide exhibit the genomic population structure of both a typical freshwater species, and a typical anadromous species. In addition to providing a first insight into the population structure of north-western European ide, our data also (1) provide indications of a single illegal introduction by man; (2) suggest limited genetic effects of heavy pollution in the past; and (3) indicate possible historical anadromous behavior in a now isolated freshwater population.

Effects of salmon lice Lepeophtheirus salmonis on wild sea trout Salmo trutta—a literature review

Salmon farming increases the abundance of salmon lice, which are ectoparasites of salmonids in the sea. Here we review the current knowledge on the effects of salmon lice on wild sea trout. Salmon lice feed on host mucus, skin and muscle, and infestation may induce osmoreg- ulatory dysfunction, physiological stress, anaemia, reduced feeding and growth, increased sus- ceptibility to secondary infections, reduced disease resistance and ultimately mortality of individ- ual sea trout. Wild sea trout in farm-free areas generally show low lice levels. In farm-intensive areas, lice levels on wild sea trout are typically higher, and more variable than in farm-free areas. Lice on wild sea trout are found at elevated levels particularly within 30 km of the nearest farms but can also extend to further ranges. Salmon lice in intensively farmed areas have negatively impacted wild sea trout populations by reducing growth and increasing marine mortality. Quan- tification of these impacts remains a challenge, although population-level effects have been quan- tified in Atlantic salmon by comparing the survival of chemically protected fish with control groups, which are relevant also for sea trout. Mortality attributable to salmon lice can lead to an average of 12�29% fewer salmon spawners. Reduced growth and increased mortality will reduce the benefits of marine migration for sea trout, and may also result in selection against anadromy in areas with high lice levels. Salmon lice-induced effects on sea trout populations may also extend to altered genetic composition and reduced diversity, and possibly to the local loss of sea trout, and establishment of exclusively freshwater resident populations.

Contrasting population genetic structure among freshwater-resident and anadromous lampreys: the role of demographic history, differential dispersal and anthropogenic barriers to movement.

The tendency of many species to abandon migration remains a poorly understood aspect of evolutionary biology that may play an important role in promoting species radiation by both allopatric and sympatric mechanisms. Anadromy inherently offers an opportunity for the colonization of freshwater environments, and the shift from an anadromous to a wholly freshwater life history has occurred in many families of fishes. Freshwater-resident forms have arisen repeatedly among lampreys (within the Petromyzontidae and Mordaciidae), and there has been much debate as to whether anadromous lampreys, and their derived freshwater-resident analogues, constitute distinct species or are divergent ecotypes of polymorphic species. Samples of 543 European river lamprey Lampetra fluviatilis (mostly from anadromous populations) and freshwater European brook lamprey Lampetra planeri from across 18 sites, primarily in the British Isles, were investigated for 13 polymorphic microsatellite DNA loci, and 108 samples from six of these sites were sequenced for 829 bp of mitochondrial DNA (mtDNA). We found contrasting patterns of population structure for mtDNA and microsatellite DNA markers, such that low diversity and little structure were seen for all populations for mtDNA (consistent with a recent founder expansion event), while fine-scale structuring was evident for nuclear markers. Strong differentiation for microsatellite DNA loci was seen among freshwater-resident L. planeri populations and between L. fluviatilis and L. planeri in most cases, but little structure was evident among anadromous L. fluviatilis populations. We conclude that postglacial colonization founded multiple freshwater-resident populations with strong habitat fidelity and limited dispersal tendencies that became highly differentiated, a pattern that was likely intensified by anthropogenic barriers.

Population structure of Coilia nasus in the Yangtze River revealed by insertion of short interspersed elements

Coilia nasus is found in the Yangtze River and the coastal waters of China, Korea, and Japan. Two ecotypes (anadromous and freshwater-resident populations) are distributed throughout the Yangtze River basin based on their ecology and behavior, but relatively little is known about the population structure of this species. Analysis of short interspersed element (SINE) insertions, which vary among individuals, has been acknowledged to provide a unique way to study population divergence. SINEs isolated from C. nasus were characterized, and this enabled analysis of the SINE insertion pattern in six populations distributed throughout the Yangtze River basin. In all populations, four SINE loci displayed individual polymorphism, and two SINE loci showed a stochastic loss in all individuals of two resident populations. The correlation between genetic and geographic populations indicated a degree of genetic isolation in this species. In contrast with Coilia grayii and Coilia mystus, two SINE loci appeared only in C. nasus. Sequencing analysis indicated that the high insertion variability of SINEs was attributed mainly to the tails, which contained various repeat copies. The results in this study will be useful for sustainable management of fishery resources and conservation of this species.

The Genetic Basis of Smoltification-Related Traits in Oncorhynchus mykiss

The timing and propensity for migration between fresh- and seawater is a key theme in the diversity of life histories within the salmonid fishes. Across salmonid species, life-history strategies range from wholly freshwater-resident populations, to migratory and nonmigratory variation within populations, to populations and species that are primarily migratory. Despite the central theme of migration to the evolution of these fishes, the genetic architecture of migration-related processes is poorly understood. Using a genetic cross of clonal lines derived from migratory and nonmigratory life-history types of Onchorhynchus mykiss (steelhead and rainbow trout, respectively), we have dissected the genetic architecture of the complex physiological and morphological transformation that occurs immediately prior to seaward migration (termed smoltification). Quantitative trait loci (QTL) analyses were used to identify the number, effects, and genomic location of loci associated with smoltification-related traits, including growth and condition factor, body coloration, morphology, and osmoregulatory enzymes during the smoltification period. Genetic analyses revealed numerous QTL, but one locus in particular is associated with multiple traits in single and joint analyses. Dissecting the genetic architecture of this highly complex trait has profound implications for understanding the genetic and evolutionary basis of life-history diversity within and among migratory fishes.

Evolutionary history of lamprey paired speciesLampetra fluviatilis(L.) andLampetra planeri(Bloch) as inferred from mitochondrial DNA variation

A remarkable trend in the evolution of lampreys is the occurrence in most genera of 'paired species', in which the parasitic anadromous lampreys are believed to have given rise to nonparasitic freshwater resident populations. The present work examines the phylogeography of the European paired species Lampetra fluviatilis and Lampetra planeri, in an attempt to elucidate species pair evolutionary history. We studied sequence variation in cytochrome b and ATPase 6, 8 mitochondrial genes in 63 individuals from 21 localities of the paired species throughout their distribution range. Results from the phylogenetic and nested clade analyses were largely consistent, suggesting the existence of three major evolutionary lineages: lineage I and possibly lineage II are widespread throughout Europe, while the most ancestral lineage III is apparently restricted to the Iberian Peninsula. The high genetic diversity observed in the Iberian Peninsula is probably the result of refugial persistence and subsequent accumulation of variation over several ice ages, whereas the low levels of genetic diversity observed in central and northern Europe should reflect a rapid postglacial colonization. Results suggest that L. planeri originated within at least two distinct evolutionary lineages, rejecting the single origin hypothesis. The observed lack of taxa monophyly within lineage I may be the result of ongoing gene flow if the two taxa are alternate life-history forms of a single species. However, structure within lineage I is also consistent with the hypothesis of divergence of taxa after postglacial dispersion (around 2000 generations ago) with incomplete lineage sorting. Further testing of the alternative hypotheses is warranted.

Conservation status of Northern Hemisphere lampreys (Petromyzontidae)

Among the 34 nominal lamprey species in the Northern Hemisphere, ten are endangered; nine are vulnerable at least in part of their range, and one is extinct. The major cause is habitat degradation through pollution and stream regulation. Four conservation priorities are recommended: 1. The protection of all lamprey species or populations thereof listed as endangered; 2. where needed, the rehabilitation of the spawning streams of non-parasitic species and the removal or circumvention of any barriers preventing access to the spawning sites; 3. the protection of permanent freshwater resident populations of anadromous species, specifically of Entosphenus tridentatus, Lampetra ayresi, L. fluviatilis, Lethenteron japonicum and Petromyzon marinus: 4. the study of the conservation status of Asian lampreys.

Meristic Differences Between Anadromous and Freshwater-Resident Arctic Char (Salvelinus alpinus) in the Sagavanirktok River Drainage, Alaska

Both anadromous and freshwater-resident populations of Arctic char (Salvelinus alpinus) occur in the Sagavanirktok River drainage, Alaska. A comparison of the gill-raker and pyloric-caeca counts of populations of the two types revealed that anadromous fish had lower gill-raker and pyloric-caeca counts than freshwater-resident fish. Freshwater-resident populations correspond meristically to McPhail's Eastern Arctic form, and anadromous population scor-respond to his Western Arctic–Bering Sea form (McPhail, J. Fish. Res. Bd. Canada 18: 793–816, 1961). It is suggested that the former was the original inhabitant of the area but has been replaced by the latter except in inaccessible, headwater lakes.