Local adaptation to salinity in the three‐spined stickleback?

Different lines of evidence suggest that the occurrence and extent of local adaptation in high gene flow marine environments – even in mobile and long‐lived vertebrates with complex life cycles – may be more widespread than earlier thought. We conducted a common garden experiment to test for local adaptation to salinity in Baltic Sea sticklebacks (Gasterosteus aculeatus). Fish from three different native salinity regimes (high, mid and low) were subjected to three salinity treatments (high, mid and low) in a full‐factorial experimental design. Irrespective of their origin, fish subjected to low (and mid) salinity treatments exhibited higher juvenile survival, grew to largest sizes and were in better condition than fish subjected to the high salinity treatment. However, a significant interaction between native and treatment salinities – resulting mainly from the poor performance of fish native to low salinity in the high salinity treatment – provided clear cut evidence for adaptation to local variation in salinity. Additional support for this inference was provided by the fact that the results concur with an earlier demonstration of significant differentiation in a number of genes with osmoregulatory functions across the same populations and that the population‐specific responses to salinity treatments exceeded that to be expected by random genetic drift.     

Salinity Adaptation and the Contribution of Parental Environmental Effects in Medicago truncatula

High soil salinity negatively influences plant growth and yield. Some taxa have evolved mechanisms for avoiding or tolerating elevated soil salinity, which can be modulated by the environment experienced by parents or offspring. We tested the contribution of the parental and offspring environments on salinity adaptation and their potential underlying mechanisms. In a two-generation greenhouse experiment, we factorially manipulated salinity concentrations for genotypes of Medicago truncatula that were originally collected from natural populations that differed in soil salinity. To compare population level adaptation to soil salinity and to test the potential mechanisms involved we measured two aspects of plant performance, reproduction and vegetative biomass, and phenological and physiological traits associated with salinity avoidance and tolerance. Saline-origin populations had greater biomass and reproduction under saline conditions than non-saline populations, consistent with local adaptation to saline soils. Additionally, parental environmental exposure to salt increased this difference in performance. In terms of environmental effects on mechanisms of salinity adaptation, parental exposure to salt spurred phenological differences that facilitated salt avoidance, while offspring exposure to salt resulted in traits associated with greater salt tolerance. Non-saline origin populations expressed traits associated with greater growth in the absence of salt while, for saline adapted populations, the ability to maintain greater performance in saline environments was also associated with lower growth potential in the absence of salt. Plastic responses induced by parental and offspring environments in phenology, leaf traits, and gas exchange contribute to salinity adaptation in M. truncatula. The ability of plants to tolerate environmental stress, such as high soil salinity, is likely modulated by a combination of parental effects and within-generation phenotypic plasticity, which are likely to vary in populations from contrasting environments.     

Trade‐offs in osmoregulation and parallel shifts in molecular function follow ecological transitions to freshwater in the Alewife

Adaptation to freshwater may be expected to reduce performance in seawater because these environments represent opposing selective regimes. We tested for such a trade‐off in populations of the Alewife (Alosa pseudoharengus). Alewives are ancestrally anadromous, and multiple populations have been independently restricted to freshwater (landlocked). We conducted salinity challenge experiments, whereby juvenile Alewives from one anadromous and multiple landlocked populations were exposed to freshwater and seawater on acute and acclimation timescales. In response to acute salinity challenge trials, independently derived landlocked populations varied in the degree to which seawater tolerance has been lost. In laboratory‐acclimation experiments, landlocked Alewives exhibited improved freshwater tolerance, which was correlated with reductions in seawater tolerance and hypo‐osmotic balance, suggesting that trade‐offs in osmoregulation may be associated with local adaptation to freshwater. We detected differentiation between life‐history forms in the expression of an ion‐uptake gene (NHE3), and in gill Na⁺/K⁺‐ATPase activity. Trade‐offs in osmoregulation, therefore, may be mediated by differentiation in ion‐uptake and salt‐secreting pathways.     

Allopatric and sympatric diversification within roach (Rutilus rutilus) of large pre‐alpine lakes

Intraspecific differentiation in response to divergent natural selection between environments is a common phenomenon in some northern freshwater fishes, especially salmonids and stickleback. Understanding why these taxa diversify and undergo adaptive radiations while most other fish species in the same environments do not, remains an open question. The possibility for intraspecific diversification has rarely been evaluated for most northern freshwater fish species. Here, we assess the potential for intraspecific differentiation between and within lake populations of roach (Rutilus rutilus)—a widespread and abundant cyprinid species—in lakes in which salmonids have evolved endemic adaptive radiations. Based on more than 3,000 polymorphic RADseq markers, we detected low but significant genetic differentiation between roach populations of two ultraoligotrophic lakes and between these and populations from other lakes. This, together with differentiation in head morphology and stable isotope signatures, suggests evolutionary and ecological differentiation among some of our studied populations. Next, we tested for intralacustrine diversification of roach within Lake Brienz, the most pristine lake surveyed in this study. We found significant phenotypic evidence for ecological intralacustrine differentiation between roach caught over a muddy substrate and those caught over a rocky substrate. However, evidence for intralacustrine genetic differentiation is at best subtle and phenotypic changes may therefore be mostly plastic. Overall, our findings suggest roach can differ between ecologically distinct lakes, but the extent of intralacustrine ecological differentiation is weak, which contrasts with the strong differentiation among endemic species of whitefish in the same lakes.     

Small Changes in Gene Expression of Targeted Osmoregulatory Genes When Exposing Marine and Freshwater Threespine Stickleback (Gasterosteus aculeatus) to Abrupt Salinity Transfers

Salinity is one of the key factors that affects metabolism, survival and distribution of fish species, as all fish osmoregulate and euryhaline fish maintain osmotic differences between their extracellular fluid and either freshwater or seawater. The threespine stickleback (Gasterosteus aculeatus) is a euryhaline species with populations in both marine and freshwater environments, where the physiological and genomic basis for salinity tolerance adaptation is not fully understood. Therefore, our main objective in this study was to investigate gene expression of three targeted osmoregulatory genes (Na⁺/K⁺-ATPase (ATPA13), cystic fibrosis transmembrane regulator (CFTR) and a voltage gated potassium channel gene (KCNH4) and one stress related heat shock protein gene (HSP70)) in gill tissue from marine and freshwater populations when exposed to non-native salinity for periods ranging from five minutes to three weeks. Overall, the targeted genes showed highly plastic expression profiles, in addition the expression of ATP1A3 was slightly higher in saltwater adapted fish and KCNH4 and HSP70 had slightly higher expression in freshwater. As no pronounced changes were observed in the expression profiles of the targeted genes, this indicates that the osmoregulatory apparatuses of both the marine and landlocked freshwater stickleback population have not been environmentally canalized, but are able to respond plastically to abrupt salinity challenges.     

Evolution of growth by genetic accommodation in Icelandic freshwater stickleback

Classical Darwinian adaptation to a change in environment can ensue when selection favours beneficial genetic variation. How plastic trait responses to new conditions affect this process depends on how plasticity reveals to selection the influence of genotype on phenotype. Genetic accommodation theory predicts that evolutionary rate may sharply increase when a new environment induces plastic responses and selects on sufficient genetic variation in those responses to produce an immediate evolutionary response, but natural examples are rare. In Iceland, marine threespine stickleback that have colonized freshwater habitats have evolved more rapid individual growth. Heritable variation in growth is greater for marine full-siblings reared at low versus high salinity, and genetic variation exists in plastic growth responses to low salinity. In fish from recently founded freshwater populations reared at low salinity, the plastic response was strongly correlated with growth. Plasticity and growth were not correlated in full-siblings reared at high salinity nor in marine fish at either salinity. In well-adapted lake populations, rapid growth evolved jointly with stronger plastic responses to low salinity and the persistence of strong plastic responses indicates that growth is not genetically assimilated. Thus, beneficial plastic growth responses to low salinity have both guided and evolved along with rapid growth as stickleback adapted to freshwater.     

Local adaptation of an anuran amphibian to osmotically stressful environments

Abstract. Water salinity is an intense physiological stress for amphibians. However, some species, such as Bufo calamita, breed in both brackish and freshwater environments. Because selection under environmentally stressful conditions can promote local adaptation of populations, we examined the existence of geographic variation in water salinity tolerance among B. calamita populations from either fresh or brackish water ponds in Southern Spain. Comparisons were made throughout various ontogenetic stages. A combination of field transplant and common garden experiments showed that water salinity decreased survival probability of individuals in all populations, prolonged their larval period, and reduced their mass at metamorphosis. However, significant population X salinity interactions indicated that the population native to brackish water (Saline) had a higher salinity tolerance than the freshwater populations, suggesting local adaptation. Saline individuals transplanted to freshwater environments showed similar survival probabilities, length of larval period, and mass at metamorphosis than those native to freshwater. This indicates that increased tolerance to osmotic stress does not imply a loss of performance in freshwater, at least during the larval and juvenile phases. Despite the adaptive process apparently undergone by Saline, all populations still shared the same upper limit of embryonic stress tolerance (around 10 g/l), defining a window of salinity range within which selection can act. Significant differences in embryonic and larval survival in brackish water among sibships for all populations suggest the existence of a genetic basis for the osmotic tolerance.     

Adaptive plasticity and genetic divergence in feeding efficiency during parallel adaptive radiation of whitefish (Coregonus spp.)

Parallel phenotypic divergence in replicated adaptive radiations could either result from parallel genetic divergence in response to similar divergent selection regimes or from equivalent phenotypically plastic response to the repeated occurrence of contrasting environments. In post‐glacial fish, replicated divergence in phenotypes along the benthic‐limnetic habitat axis is commonly observed. Here, we use two benthic‐limnetic species pairs of whitefish from two Swiss lakes, raised in a common garden design, with reciprocal food treatments in one species pair, to experimentally measure whether feeding efficiency on benthic prey has a genetic basis or whether it underlies phenotypic plasticity (or both). To do so, we offered experimental fish mosquito larvae, partially burried in sand, and measured multiple feeding efficiency variables. Our results reveal both, genetic divergence as well as phenotypically plastic divergence in feeding efficiency, with the phenotypically benthic species raised on benthic food being the most efficient forager on benthic prey. This indicates that both, divergent natural selection on genetically heritable traits and adaptive phenotypic plasticity, are likely important mechanisms driving phenotypic divergence in adaptive radiation.     

Local adaptation and phenotypic plasticity both occurred in <Emphasis Type="Italic">Wedelia trilobata</Emphasis> invasion across a tropical island

The role of the local adaptation and phenotypic plasticity of invasive species in their invasion of new environments has historically been a debatable issue, particularly at small spatial scales (e.g., different habitats within an island). We selected seven field sites across Hainan Island, Hainan Province, China, to investigate the role of local adaptation and/or phenotypic plasticity in the successful invasion of Wedelia trilobata by a field survey, molecular marker analysis, and common garden experiment. In the field survey, the clonal growth characteristics of W. trilobata showed significant differences among the seven sites, suggesting that the species was able to adapt to different environments. The mean phenotypic plasticity index of W. trilobata was higher than that of other invasive plant species (0.61 vs 0.48). The analysis of the inter-simple sequence repeat molecular markers of 420 individuals from the seven sites revealed a Shannon’s index that was similar to those of other invasive plants (0.29 vs 0.25). The nested analysis of the molecular variance in the genetic diversity of the population showed significant differences among the sites. In the common garden experiment, the growth characteristics of plants grown from the seven sites were significantly affected by light and density treatments but not by soil moisture. However, the responses of plants grown from different sites to light treatment varied. Plants from sunny sites had greater clonal traits than those from shady sites, indicating that local adaptation occurred in plant populations grown at some sites. Overall, our results implied that both phenotypic plasticity and local adaptation contributed to the successful invasion of W. trilobata across Hainan Island.     

Parallel and non‐parallel morphological divergence among foraging specialists in European whitefish (Coregonus lavaretus)

Parallel phenotypic evolution occurs when independent populations evolve similar traits in response to similar selective regimes. However, populations inhabiting similar environments also frequently show some phenotypic differences that result from non‐parallel evolution. In this study, we quantified the relative importance of parallel evolution to similar foraging regimes and non‐parallel lake‐specific effects on morphological variation in European whitefish (Coregonus lavaretus). We found evidence for both lake‐specific morphological characteristics and parallel morphological divergence between whitefish specializing in feeding on profundal and littoral resources in three separate lakes. Foraging specialists expressed similar phenotypes in different lakes in both overall body shape and selected measured morphological traits. The morphology of the two whitefish specialists resembled that predicted from other fish species, supporting the conclusion of an adaptive significance of the observed morphological characteristics. Our results indicate that divergent natural selection resulting from foraging specialization is driving and/or maintaining the observed parallel morphological divergence. Whitefish in this study may represent an early stage of divergence towards the evolution of specialized morphs.     

Intraspecific variation in gene expression after seawater transfer in gills of the euryhaline killifish Fundulus heteroclitus

Previous research has suggested that northern populations of the euryhaline killifish (Fundulus heteroclitus) are better adapted to freshwater environments than their southern counterparts. In this study, we examined whether this adaptation has come at an ionoregulatory cost in seawater, by comparing published data for northern killifish to newly acquired data on the molecular responses of southern killifish to seawater transfer. After abrupt transfer from brackish water (10 per thousand) to seawater, Na,K-ATPase activity, Na,K-ATPase alpha(1a) mRNA expression, and NKCC1 mRNA expression increased 1 and 4 days after transfer in the gills of southern fish (by 2-3-fold), but increased at 1 day and not 4 days after transfer in northern fish. Small increases in mRNA expression were observed in both populations at 14 days. CFTR expression also increased in southern and northern fish at 1 and 4 days into seawater, and was also elevated at 14 days in northern fish. Because fish from both southern and northern populations maintained plasma Na(+) and Cl(-) balance after seawater transfer, the differences in activity and expression could not have been caused by differences in plasma ion levels. Instead, some other regulatory factor may account for the differences in expression between populations. This study shows that freshwater adaptation in northern populations of killifish has not necessarily come at a significant ionoregulatory cost in seawater, but has altered the molecular responses of their gills to seawater transfer compared to southern killifish.     

Laboratory simulation of the effects of environmental salinity on wild‐caught juveniles of European sea bass Dicentrarchus labrax and gilthead seabream Sparus aurata

Gilthead seabream Sparus aurata and European sea bass Dicentrarchus labrax , are two important species in Mediterranean aquaculture. In the wild, their juveniles occur in brackish areas such as lagoons and river deltas. Even though the juveniles seem to favour brackish environments, low salinity incurs an energy cost for osmoregulation. This paper presents the results of a series of laboratory experiments exploring the effects of salinity on growth, feeding, food conversion, survival and maintenance energy requirements of wild‐caught juveniles. The fish were kept in the laboratory, divided in groups of 20 in small tanks of 50 l each, and supplied with biologically filtered seawater of four salinity levels (8, 18, 28‰ and natural seawater) and fixed temperature (20 ± 1·4° C). The fish were fed pelleted feed throughout the experiment. Both species showed great similarity in their responses to lower salinities. Satiation time for both species increased with decreasing salinity, while maintenance requirements (required daily ration and energy) increased as with increasing salinity. Growth and feed conversion is highest for salinities around 28‰ and lower for salinities above and below. Both species share common physiological features, and intermediate salinities are optimal for their performance in nature and in captivity.     

Variable salinity tolerance in ascidian larvae is primarily a plastic response to the parental environment

Both phenotypic plasticity and local genetic adaptation may contribute to a species’ ability to inhabit different environmental conditions. While phenotypic plasticity is usually considered costly, local adaptation takes generations to respond to environmental change and may be constrained by strong gene flow. The majority of marine species have complex life-cycles with pelagic stages that might be expected to promote gene flow and plastic responses, and yet several notable examples of local adaptation have been found in species with broadcast larvae. In the ascidian, Ciona intestinalis (Linnaeus, 1767),—a common marine species with broadcast spawning and a short larval stage—previous studies have found marked differences in salinity tolerance of early life-history stages among populations from different salinity regimes. We used common-garden experiments to test whether observed differences in salinity tolerance could be explained by phenotypic plasticity. Adult ascidians from two low salinity populations [2–5 m depth, ~25 practical salinity units (PSU)], and two full salinity populations (25–27 m depth, ~31 PSU) were acclimated for 2–4 weeks at both 25 and 31 PSU. Gametes were fertilized at the acclimation salinities, and the newly formed embryos were transferred to 10 different salinities (21–39 PSU) and cultured to metamorphosis. Adult acclimation salinity had an overriding and significant effect on larval metamorphic success: tolerance norms for larvae almost fully matched the acclimation salinity of the parents, independent of parental origin (deep or shallow). However we also detected minor population differences that could be attributed to either local adaptation or persistent environmental effects. We conclude that differences in salinity tolerance of C. intestinalis larvae from different populations are driven primarily by transgenerational phenotypic plasticity, a strategy that seems particularly favourable for an organism living in coastal waters where salinity is less readily predicted than in the open oceans.     

Cryptic genetic variation and body size evolution in threespine stickleback

The role of environment as a selective agent is well-established. Environment might also influence evolution by altering the expression of genetic variation associated with phenotypes under selection. Far less is known about this phenomenon, particularly its contribution to evolution in novel environments. We investigated how environment affected the evolvability of body size in the threespine stickleback (Gasterosteus aculeatus). Gasterosteus aculeatus is well suited to addressing this question due to the rapid evolution of smaller size in the numerous freshwater populations established following the colonization of new freshwater habitats by an oceanic ancestor. The repeated, rapid evolution of size following colonization contrasts with the general observation of low phenotypic variation in oceanic stickleback. We reared an oceanic population of stickleback under high and low salinity conditions, mimicking a key component of the ancestral environment, and freshwater colonization, respectively. There was low genetic variation for body size under high salinity, but this variance increased significantly when fish were reared under low salinity. We therefore conclude that oceanic populations harbor the standing genetic variation necessary for the evolution of body size, but that this variation only becomes available to selection upon colonization of a new habitat.     

New insights into fish ion regulation and mitochondrion-rich cells

Compared to terrestrial animals, fish have to cope with more-challenging osmotic and ionic gradients from aquatic environments with diverse salinities, ion compositions, and pH values. Gills, a unique and highly studied organ in research on fish osmoregulation and ionoregulation, provide an excellent model to study the regulatory mechanisms of ion transport. The present review introduces and discusses some recent advances in relevant issues of teleost gill ion transport and functions of gill ionocytes. Based on accumulating evidence, a conclusive model of NaCl secretion in gills of euryhaline teleosts has been established. Interpretations of results of studies on freshwater fish gill Na+/Cl- uptake mechanisms are still being debated compared with those for NaCl secretion. Current models for Na+/Cl- uptake are proposed based on studies in traditionally used model species. Many reported inconsistencies are claimed to be due to differences among species, various experimental designs, or acclimation conditions. Having the benefit of advanced techniques in molecular/cellular biology, functional genomics, and model animals, several new notions have recently been raised concerning relevant issues of Na+/Cl- uptake pathways. Several new windows have been opened particularly in terms of molecular mechanisms of ionocyte differentiation and energy metabolite transport between gill cells during environmental challenge.     

Evolutionary mismatch along salinity gradients in a Neotropical water strider

The evolution of local adaptation is crucial for the in situ persistence of populations in changing environments. However, selection along broad environmental gradients could render local adaptation difficult, and might even result in maladaptation. We address this issue by quantifying fitness trade‐offs (via common garden experiments) along a salinity gradient in two populations of the Neotropical water strider Telmatometra withei—a species found in both fresh (FW) and brackish (BW) water environments across Panama. We found evidence for local adaptation in the FW population in its home FW environment. However, the BW population showed only partial adaptation to the BW environment, with a high magnitude of maladaptation along naturally occurring salinity gradients. Indeed, its overall fitness was ~60% lower than that of the ancestral FW population in its home environment, highlighting the role of phenotypic plasticity, rather than local adaptation, in high salinity environments. This suggests that populations seemingly persisting in high salinity environments might in fact be maladapted, following drastic changes in salinity. Thus, variable selection imposed by salinization could result in evolutionary mismatch, where the fitness of a population is displaced from its optimal environment. Understanding the fitness consequences of persisting in fluctuating salinity environments is crucial to predict the persistence of populations facing increasing salinization. It will also help develop evolutionarily informed management strategies in the context of global change.     

Ecological correlates of the distribution limits of two poeciliid species along a salinity gradient

Identifying the environmental factors responsible for the formation of a species' distribution limit is challenging because organisms interact in complex ways with their environments. However, the use of statistical niche models in combination with the analysis of phenotypic variation along environmental gradients can help to reduce such complexity and identify a subset of candidate factors. In the present study, we used such approaches to describe and identify factors responsible for the parapatric distribution of two closely‐related livebearer fish species along a salinity gradient in the lowlands of Trinidad, West Indies. The downstream distribution limits of Poecilia reticulata were strongly correlated with the brackish–freshwater interface. We did not observe significant phenotypic variation in life‐history traits for this species when comparing marginal with more central populations, suggesting that abrupt changes in conditions at the brackish–freshwater interface limit its distribution. By contrast, Poecilia picta was present across a wide range of salinities, although it gradually disappeared from upstream freshwater localities. In addition, P. picta populations exhibited an increase in offspring size in localities where they coexist with P. reticulata, suggesting a role for interspecific competition. The parapatric distribution of these two species, suggests that P. reticulata distributions are limited by an abiotic factor (salinity), whereas P. picta is limited by a biotic factor (interspecific competition). Similar parapatric patterns have been previously described in other systems, suggesting they might be a common pattern in nature. © 2013 The Linnean Society of London