Allometric relationships in morphological traits associated with foraging,swimming ability,and predator defense reveal adaptations toward brackish and freshwater environments in the threespine stickleback

Freshwater colonization by threespine stickleback has led to divergence in morphology between ancestral marine and derived freshwater populations, making them ideal for studying natural selection on phenotypes. In an open brackish–freshwater system, we previously discovered two genetically distinct stickleback populations that also differ in geometric shape: one mainly found in the brackish water lagoon and one throughout the freshwater system. As shape and size are not perfectly correlated, the aim of this study was to identify the morphological trait(s) that separated the populations in geometric shape. We measured 23 phenotypes likely to be important for foraging, swimming capacity, and defense against predation. The lateral plate morphs in freshwater displayed few significant changes in trait sizes, but the low plated expressed feeding traits more associated with benthic habitats. When comparing the completely plated genetically assigned populations, the freshwater, the hybrids, the migrants and the lagoon fish, many of the linear traits had different slopes and intercepts in trait‐size regressions, precluding our ability to directly compare all traits simultaneously, which most likely results from low variation in body length for the lagoon and migrant population. We found the lagoon stickleback population to be more specialized toward the littoral zone, displaying benthic traits such as large, deep bodies with smaller eyes compared to the freshwater completely plated morph. Further, the lagoon and migrant fish had an overall higher body coverage of lateral plates compared to freshwater fish, and the dorsal and pelvic spines were longer. Evolutionary constraints due to allometric scaling relationships could explain the observed, overall restricted, differences in morphology between the sticklebacks in this study, as most traits have diversified in common allometric trajectories. The observed differences in foraging and antipredation traits between the fish with a lagoon and freshwater genetic signature are likely a result of genetic or plastic adaptations toward brackish and freshwater environments.     

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.     

Sex differentiation of the European eel in brackish and freshwater environments: a comparative analysis

Body growth parameters, age and total length at sex differentiation were compared in three European eel Anguilla anguilla populations from Mediterranean sites with different salinity. Whilst body growth was faster in brackish than in freshwater environments, the present analysis shows that body size at sex differentiation might be a physiological invariant.     

Genetic and morphometric divergence in threespine stickleback in the Chignik catchment,Alaska

Divergent selection pressures induced by different environmental conditions typically lead to variation in life history, behavior, and morphology. When populations are locally adapted to their current environment, selection may limit movement into novel sites, leading to neutral and adaptive genetic divergence in allopatric populations. Subsequently, divergence can be reinforced by development of pre‐ or postzygotic barriers to gene flow. The threespine stickleback, Gasterosteus aculeatus, is a primarily marine fish that has invaded freshwater repeatedly in postglacial times. After invasion, the established freshwater populations typically show rapid diversification of several traits as they become reproductively isolated from their ancestral marine population. In this study, we examine the genetic and morphometric differentiation between sticklebacks living in an open system comprising a brackish water lagoon, two freshwater lakes, and connecting rivers. By applying a set of microsatellite markers, we disentangled the genetic relationship of the individuals across the diverse environments and identified two genetic populations: one associated with brackish and the other with the freshwater environments. The “brackish” sticklebacks were larger and had a different body shape than those in freshwater. However, we found evidence for upstream migration from the brackish lagoon into the freshwater environments, as fish that were genetically and morphometrically similar to the lagoon fish were found in all freshwater sampling sites. Regardless, few F1‐hybrids were identified, and it therefore appears that some pre‐ and/or postzygotic barriers to gene flow rather than geographic distance are causing the divergence in this system.     

Effects of salinity on the life history and fitness of Daphnia magna: variability within and between populations

The life history traits of Daphnia magna were studied in laboratory experiments under freshwater and brackish (5 salinity) conditions. The variability of responses within and between populations was examined by comparing 11 clones from a brackish lake and 10 clones from a freshwater pond. Experimental clones were hatched from ephippia collected from the sediment and thus represent random samples of the clone banks of each population.Most clones with a high salinity tolerance were from the population of the brackish habitat, but some were also found in the freshwater population. Thus, freshwater populations appear to have the potential to invade brackish habitats. A proportion of clones from the brackish population had very low fitness (measured as e^r) under freshwater conditions. This unexpected result means that freshwater adaptation can be lost by the freshwater cladoceran Daphnia magna. The effects of unfavourable conditions on growth and reproduction varied among clones and were not correlated. This clonal variation in growth and reproduction indicates that the environmental sensitivities of these traits are independent. The pattern of fitness reaction norms showed no trade-off between fitness under brackish and under freshwater conditions for either population. Thus, euryhaline generalists should be favoured in habitats with salinity fluctuations between freshwater and brackish conditions.     

Evidence of prezygotic isolation,but not assortative mating,between locally adapted populations of Fundulus heteroclitus across a salinity gradient

Selection along environmental gradients can drive reproductive isolation and speciation. Among fishes, salinity is a major factor limiting species distributions, and despite its importance in generating species diversity, speciation events between marine and freshwater are rare. Here, we tested for mechanisms of reproductive isolation between locally adapted freshwater and brackish water-native populations of killifish, Fundulus heteroclitus, from either side of a hybrid zone along a salinity gradient. There was evidence for pre-zygotic endogenous reproductive isolation with reduced fertilization success between crosses of freshwater-native males and brackish water-native females. Exogenous pre-zygotic isolation was also present where females had highest fertilization in their native salinity. We used a replicated mass spawning design to test for mate choice in both brackish and fresh water. After genotyping 187 parents and 2523 offspring at 2347 SNPs across the genome, 85% of offspring were successfully assign to their parents. However, no reinforcing mate choice was observed. These results therefore demonstrate emerging, yet limited, reproductive isolation and incipient speciation across a marine to freshwater salinity gradient and suggest that both endogenous and exogenous mechanisms, but not assortative mating, contribute to divergence.     

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     

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.     

Genotype-by-environment interaction for salinity tolerance in the freshwater-invading copepod Eurytemora affinis

This study examined the extent of phenotypic plasticity for salinity tolerance and genetic variation in plasticity in the invasive copepod Eurytemora affinis. Euryemora affinis is a species complex inhabiting brackish to hypersaline environments but has invaded freshwater lakes and reservoirs within the past century. Reaction norm experiments were performed on a relatively euryhaline population collected from a brackish lake with fluctuating salinity. Life history traits (hatching rate, survival, and development time) were measured for 20 full-sib clutches that were split and reared at four salinities (fresh, 5, 10, and 27 practical salinity units [PSU]). On average, higher salinities (10 and 27 PSU) were more favorable for larval growth, yielding greater survival and faster development rate. Clutches differed significantly in their response to salinity, with a significant genotype-by-environment interaction for development time. In addition, genetic (clutch) effects were evident in response to low salinity, given that survival in fresh (lake) water was significantly positively correlated with survival at 5 PSU for individual clutches. Clutches raised in fresh water could not survive beyond metamorphosis, suggesting that acclimation to fresh water could not occur in a single generation. Results suggest the importance of natural selection during freshwater invasion events, given the inability of plasticity to generate a freshwater phenotype, and the presence of genetic variation for plasticity upon which natural selection could act.     

Phenotypic plasticity in growth and fecundity induced by strong population fluctuations affects reproductive traits of female fish

Fish are known for their high phenotypic plasticity in life‐history traits in relation to environmental variability, and this is particularly pronounced among salmonids in the Northern Hemisphere. Resource limitation leads to trade‐offs in phenotypic plasticity between life‐history traits related to the reproduction, growth, and survival of individual fish, which have consequences for the age and size distributions of populations, as well as their dynamics and productivity. We studied the effect of plasticity in growth and fecundity of vendace females on their reproductive traits using a series of long‐term incubation experiments. The wild parental fish originated from four separate populations with markedly different densities, and hence naturally induced differences in their growth and fecundity. The energy allocation to somatic tissues and eggs prior to spawning served as a proxy for total resource availability to individual females, and its effects on offspring survival and growth were analyzed. Vendace females allocated a rather constant proportion of available energy to eggs (per body mass) despite different growth patterns depending on the total resources in the different lakes; investment into eggs thus dictated the share remaining for growth. The energy allocation to eggs per mass was higher in young than in old spawners and the egg size and the relative fecundity differed between them: Young females produced more and smaller eggs and larvae than old spawners. In contrast to earlier observations of salmonids, a shortage of maternal food resources did not increase offspring size and survival. Vendace females in sparse populations with ample resources and high growth produced larger eggs and larvae. Vendace accommodate strong population fluctuations by their high plasticity in growth and fecundity, which affect their offspring size and consequently their recruitment and productivity, and account for their persistence and resilience in the face of high fishing mortality.     

Cryptic freshwater ciliates in a hypersaline lagoon

Ubiquitous dispersal of free-living microbial species implies that each and every ecosystem supports a ‘seedbank’ of microbial species that are imported by random dispersal. However, many of the microbial species present in any particular ecosystem will probably never thrive there because the local environment is unsuitable for their population growth. To test this, we investigated the ciliated protozoa in a hypersaline lagoon in Almería, Spain, using selective enrichment to reveal typical freshwater species, as the ‘signature’ of random dispersal. Twenty-four ciliate species, 14 of them not previously recorded from hypersaline waters, were identified in the undiluted waters of the lagoon. But when the salinity was gradually diluted, further species typical of fresh- and brackish waters emerged, indicating that they had persisted in a viable state at the previously high salinity. These additional species increased the recorded ciliate species total for the lagoon to 36. The species found in the lagoon appeared to be adapted to either high, or variable, or low salinity, implying that they may have originated in a variety of habitats that differed greatly with respect to salinity regime.     

Adaptation to sea level rise: does local adaptation influence the demography of coastal fish populations?

This study compared the growth of two western mosquitofish Gambusia affinis populations that were previously demonstrated to have genetic adaptations that increased survival under lethal salinity exposures. The objective was to evaluate how genetic adaptations to lethal salinity stress affect population demography when exposed to sublethal salinity stress. Results indicate that chronic salinity exposure had a generally negative impact on population size, but fish originating from one of the two populations established with fish from a brackish site exhibited an increase in population size. Saltwater intrusion seems to result in reduced population size for most populations. Some populations inhabiting more saline sites, however, may develop localized adaptations, mitigating the consequences of increased salinity on population productivity.     

Elongation and mat formation of <Emphasis Type="Italic">Chara aspera</Emphasis> under different light and salinity conditions

Former laboratory results indicate that shoot elongation at low light intensities of Chara aspera is absent already at 10 psu which is within the physiologically optimal salinity range for brackish water populations. To investigate if similar restrictions occur in the field, density and morphology of C. aspera were compared between three freshwater and three brackish water sites along its depth range. The lower depth limit of C. aspera varied considerably among sites (30–600 cm) related to turbidity. Light availability at the lower depth limit corresponded to about 15% of surface irradiance in freshwater and brackish water with lower salinity (3.4 psu). Total length increased and fresh weight:length ratio decreased with depth at these sites indicating shoot elongation related to lower light availability. Due to shoot elongation, light availability was far higher at the upper parts of the shoot than at the bottom in the turbid sites. Light availability at the lower depth limit was higher (about 40%) at two sites with higher salinity (7–8 psu), where no shoot elongation was observed at the lower depth limit. Instead, the plants were stunted and often covered with filamentous algae or shaded by other rooted submerged macrophytes indicating competitive disadvantages of C. aspera at higher salinities. As growth in high densities (mat formation) exposes the plants to severe self-shading, it is suggested that shoot elongation is a prerequisite to mat formation. Dense vegetation of C. aspera was found only in freshwater and brackish water with lower salinity. Single, richly branched plants occurred in clearwater sites with higher salinity. C. aspera was not found in “double stress” environments with both high turbidity and high salinity: We asume that the species is a poor competitor under these conditions. Our results indicate that morphological differences between freshwater and brackish water populations of C. aspera are at least partly explained by salinity rather than genetic differences.     

The growth of pikeperch (Sander lucioperca L.) and perch (Perca fluviatilis L.) under different water temperature and salinity conditions in the Curonian Lagoon and Lithuanian coastal waters of the Baltic Sea

Pikeperch and perch perform seasonal migrations between the Curonian Lagoon and the coastal waters of the Baltic Sea. The Curonian Lagoon is a freshwater basin, while salinity in the coastal waters varies between of 4.9–6.8 psu. In the Curonian Lagoon water temperature is generally higher than in the coastal waters. Field studies of growth and condition characteristics of pikeperch and perch were carried out in these water bodies with the aim to estimate growth differences of the two fish species under different salinity and temperature conditions. Additionally, an experimental study of the impact of salinity on the growth of perch young-of-the-year (YOY) was performed to test the hypothesis that a brackish environment positively influences percids. Field observations revealed that body length, condition factor, fatness coefficient and fat content in muscles were significantly higher in individuals inhabiting the cooler, brackish waters of the Baltic Sea than in individuals inhabiting the Curonian Lagoon. A positive effect of low salinity on growth was also established in the experimental study. Hence, the study results suggest that under certain temperature conditions, brackish waters beneficially affect the growth of pikeperch and perch.     

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.     

Ecophysiological differences of betaproteobacterial populations in two hydrochemically distinct compartments of a subtropical lagoon

We studied the population sizes and substrate incorporation patterns of three phylogenetic groups of Betaproteobacteria in a coastal subtropical lagoon that is characterized by a sharp transition from humic freshwater to turbid brackish water. Various cellular processes were addressed by short-term incubations with four radiolabelled compounds and microautoradiographic assessment of substrate incorporation. Group-specific differences in the abundances and the respective physiological state of the three populations were observed upon transfer from the humic-rich compartment to the main body of the lagoon (estimated at 1–2 days). Members of the clade B of Polynucleobacter (PnecB) experienced only an insignificant change in cell numbers, but displayed a general metabolic downshift, carbon metabolism (glucose incorporation) being most affected. By contrast, bacteria from the closely related Polynucleobacter C clade (PnecC) clearly differed in total abundances and in the numbers of DNA-synthesizing or glucose incorporating cells. At the same time, PnecC bacteria maintained comparable levels of protein synthesis (leucine uptake) in both lagoon compartments, and the proportion of cells incorporating N -acetylglucosamine was even higher in the main body of the lagoon. Members of the R-BT lineage showed little changes in cell numbers, DNA synthesis and carbon metabolism. Altogether, the observed patterns of substrate metabolism suggest that different bacterial populations in the lagoon undergo specific physiological adjustments in response to changing environmental conditions.     

Contrasting patterns of quantitative and neutral genetic variation in locally adapted populations of the natterjack toad, Bufo calamita

The relative importance of natural selection and genetic drift in determining patterns of phenotypic diversity observed in nature is still unclear. The natterjack toad (Bufo calamita) is one of a few amphibian species capable of breeding in saline ponds, even though water salinity represents a considerable stress for them. Results from two common-garden experiments showed a pattern of geographic variation in embryonic salinity tolerance among populations from either fresh or brackish environments, consistent with the hypothesis of local adaptation. Full-sib analysis showed increased variation in survival among sibships within population for all populations as osmotic stress was increased (broad-sense heritability increased as salinity raised). Nevertheless, toads native to the brackish water environment had the highest overall survival under brackish conditions. Levels of population genetic differentiation for salinity tolerance were higher than those of neutral genetic differentiation, the latter obtained through the analysis of eight microsatellite loci. Microsatellite markers also revealed little population differentiation, lack of an isolation-by-distance pattern, and moderate gene flow connecting the populations. Therefore, environmental stress tolerance appears to have evolved in absence of geographic isolation, and consequently we reject the null hypothesis of neutral differentiation.     

Influence of changes in salinity and light intensity on growth of phytoplankton communities from the Schelde river and estuary (Belgium/The Netherlands)

In the Schelde continuum, a succession in the phytoplankton community is observed along the transition from the river to the freshwater tidal reaches of the estuary and from the freshwater to brackish reaches of the estuary. The goal of this study was to experimentally evaluate the contribution of changes in salinity and light climate to this succession. In summer 2000 and in spring 2001, phytoplankton communities from the river, the freshwater tidal reaches and the brackish reaches of the estuary were incubated under high or low light intensities and exposed to a change in salinity. HPLC analysis was used to evaluate the response of different algal groups to changes in light intensity and salinity. When incubated at a light intensity corresponding to the mean underwater light intensity of the freshwater tidal reaches, growth of phytoplankton from the river as well as from freshwater tidal reaches was significantly lower than when incubated at a light intensity corresponding to the mean underwater light intensity of the river. The phytoplankton community from the freshwater tidal reaches did not appear to be better adapted to low light intensities than the phytoplankton community from the river. Although diatoms were expected to be less sensitive to a reduction in light intensity than green algae, the opposite response was observed. Freshwater and brackish water phytoplankton were negatively affected by respectively an increase or decrease in salinity. However, the effect of salinity was not strong enough to explain the disappearance of freshwater and brackish water phytoplankton between a salinity of 0.5 and 10 psu, suggesting that other factors also play a role. In the freshwater phytoplankton communities from the river and the freshwater tidal reaches, green algae and diatoms responded in a similar way to an increase in salinity. In the brackish water phytoplankton community, fucoxanthin displayed a different response to salinity than lutein and chlorophyll a.     

Phenotypic plasticity and contemporary evolution in introduced populations: evidence from translocated populations of white sands pupfish (<Emphasis Type="Italic">Cyrpinodon tularosa</Emphasis>)

Contemporary evolution has been shown in a few studies to be an important component of colonization ability, but seldom have researchers considered whether phenotypic plasticity facilitates directional evolution from the invasion event. In the current study, we evaluated body shape divergence of the New Mexico State-threatened White Sands pupfish (Cyprinodon tularosa) that were introduced to brackish, lacustrine habitats at two different time in the recent past (approximately 30 years and 1 year previously) from the same source population (saline river environment). Pupfish body shape is correlated with environmental salinity: fish from saline habitats are characterized by slender body shapes, whereas fish from fresher, yet brackish springs are deep-bodied. In this study, lacustrine populations consisted of an approximately 30-year old population and several 1-year old populations, all introduced from the same source. The body shape divergence of the 30-year old population was significant and greater than any of the divergences of the 1-year old populations (which were for the most part not significant). Nonetheless, all body shape changes exhibited body deepening in less saline environments. We conclude that phenotypic plasticity potentially facilitates directional evolution of body deepening for introduced pupfish populations.     

Quantitative genetic and translocation experiments reveal genotype‐by‐environment effects on juvenile life‐history traits in two populations of Chinook salmon (Oncorhynchus tshawytscha)

Understanding the genetic architecture of phenotypic plasticity is required to assess how populations might respond to heterogeneous or changing environments. Although several studies have examined population‐level patterns in environmental heterogeneity and plasticity, few studies have examined individual‐level variation in plasticity. Here, we use the North Carolina II breeding design and translocation experiments between two populations of Chinook salmon to detail the genetic architecture and plasticity of offspring survival and growth. We followed the survival of 50 800 offspring through the larval stage and used parentage analysis to examine survival and growth through freshwater rearing. In one population, we found that additive genetic, nonadditive genetic and maternal effects explained 25%, 34% and 55% of the variance in larvae survival, respectively. In the second population, these effects explained 0%, 24% and 61% of the variance in larvae survival. In contrast, fry survival was regulated primarily by additive genetic effects, which indicates a shift from maternal to genetic effects as development proceeds. Fry growth also showed strong additive genetic effects. Translocations between populations revealed that offspring survival and growth varied between environments, the degree of which differed among families. These results indicate genetic differences among individuals in their degree of plasticity and consequently their ability to respond to environmental variation.