Growth portfolios buffer climate-linked environmental change in marine systems.

Large-scale, climate-induced synchrony in the productivity of fish populations is becoming more pronounced in the world's oceans. As synchrony increases, a population's "portfolio" of responses can be diminished, in turn reducing its resilience to strong perturbation. Here we argue that the costs and benefits of trait synchronization, such as the expression of growth rate, are context dependent. Contrary to prevailing views, synchrony among individuals could actually be beneficial for populations if growth synchrony increases during favorable conditions, and then declines under poor conditions when a broader portfolio of responses could be useful. Importantly, growth synchrony among individuals within populations has seldom been measured, despite well-documented evidence of synchrony across populations. Here, we used century-scale time series of annual otolith growth to test for changes in growth synchronization among individuals within multiple populations of a marine keystone species (Atlantic cod, Gadus morhua). On the basis of 74,662 annual growth increments recorded in 13,749 otoliths, we detected a rising conformity in long-term growth rates within five northeast Atlantic cod populations in response to both favorable growth conditions and a large-scale, multidecadal mode of climate variability similar to the East Atlantic Pattern. The within-population synchrony was distinct from the across-population synchrony commonly reported for large-scale environmental drivers. Climate-linked, among-individual growth synchrony was also identified in other Northeast Atlantic pelagic, deep-sea and bivalve species. We hypothesize that growth synchrony in good years and growth asynchrony in poorer years reflects adaptive trait optimization and bet hedging, respectively, that could confer an unexpected, but pervasive and stabilizing, impact on marine population productivity in response to large-scale environmental change.

Disparate movement behavior and feeding ecology in sympatric ecotypes of Atlantic cod.

Coexistence of ecotypes, genetically divergent population units, is a widespread phenomenon, potentially affecting ecosystem functioning and local food web stability. In coastal Skagerrak, Atlantic cod (Gadus morhua) occur as two such coexisting ecotypes. We applied a combination of acoustic telemetry, genotyping, and stable isotope analysis to 72 individuals to investigate movement ecology and food niche of putative local "Fjord" and putative oceanic "North Sea" ecotypes-thus named based on previous molecular studies. Genotyping and individual origin assignment suggested 41 individuals were Fjord and 31 were North Sea ecotypes. Both ecotypes were found throughout the fjord. Seven percent of Fjord ecotype individuals left the study system during the study while 42% of North Sea individuals left, potentially homing to natal spawning grounds. Home range sizes were similar for the two ecotypes but highly variable among individuals. Fjord ecotype cod had significantly higher δ13C and δ15N stable isotope values than North Sea ecotype cod, suggesting they exploited different food niches. The results suggest coexisting ecotypes may possess innate differences in feeding and movement ecologies and may thus fill different functional roles in marine ecosystems. This highlights the importance of conserving interconnected populations to ensure stable ecosystem functioning and food web structures.

Differences in metabolic rate between two Atlantic cod (Gadus morhua) populations estimated with carbon isotopic composition in otoliths.

The isotopic composition of inorganic carbon in otoliths (δ13Coto) can be a useful tracer of metabolic rates and a method to study ecophysiology in wild fish. We evaluated environmental and physiological sources of δ13Coto variation in Icelandic and Northeast Arctic (NEA) cod (Gadus morhua) over the years 1914-2013. Individual annual growth increments of otoliths formed at age 3 and 8 were micromilled and measured by isotope-ratio mass spectrometry. Simultaneously, all annual increment widths of the otoliths were measured providing a proxy of fish somatic growth. We hypothesized that changes in the physiological state of the organism, reflected by the isotopic composition of otoliths, can affect the growth rate. Using univariate and multivariate mixed-effects models we estimated conditional correlations between carbon isotopic composition and growth of fish at different levels (within individuals, between individuals, and between years), controlling for intrinsic and extrinsic effects on both otolith measurements. δ13Coto was correlated with growth within individuals and between years, which was attributed to the intrinsic effects (fish age or total length). There was no significant correlation between δ13Coto and growth between individuals, which suggests that caution is needed when interpreting δ13Coto signals. We found a significant decrease in δ13Coto through the century which was explained by the oceanic Suess effect-admixture of isotopically light carbon from fossil fuel. We calculated the proportion of the respired carbon in otolith carbonate (Cresp) using carbon isotopic composition in diet and dissolved inorganic carbon of the seawater. This approach allowed us to correct the values for each stock in relation to these two environmental baselines. Cresp was on average 0.275 and 0.295 in Icelandic and NEA stock, respectively. Our results provide an insight into the physiological basis for differences in growth characteristics between these two cod stocks, and how that may vary over time.

Intra-annual variation in feeding of Atlantic cod Gadus morhua: the importance of ephemeral prey bursts.

Seasonal prey bursts are important for the life cycles and energy budgets of many predators. This study documents the diet and, especially, the importance of the ephemeral occurrence of capelin as prey for Atlantic cod (Gadus morhua) in Godthaabsfjord, west Greenland, over an annual cycle. The cod showed clear differences in diet composition on the 11 sampling dates resulting in a spring-summer, late summer-autumn and winter cluster. Moreover, a single sampling date, 12 May, was defined by cod gorge feeding on spawning capelin, which led to average stomach contents 4.3 times higher than the average for the remaining sampling dates. Changes in nitrogen stable isotope values from 22 April to 7 July in cod liver and muscle tissue were used to calculate the consumption of capelin. Based on this, the consumption of capelin varied between 538 and 658 g wet weight for a 1.3 kg cod. Using published consumption/biomass estimates and observed growth rates, the capelin intake corresponds to 10.1%-33.3% of the annual food consumption and accounts for 28.1%-34.5% of the annual growth of the cod. The present study documents the omnivorous feeding mode of Atlantic cod but highlights the utilization and importance of ephemeral prey bursts for the annual energy budget of the cod. It is hypothesized that access to capelin is critical for the postspawning recovery of Godthaabsfjord cod.

Temporal changes in size-at-maturity of black dogfish Centroscyllium fabricii.

By examining the maturity of 283 black dogfish Centroscyllium fabricii from Greenland waters, a shift in size-at-maturity in both sexes over the past 25 years is observed. Size-at-first maturity decreased approximately 10 cm in both sexes, and L50 and L95 shifted similarly in males, but not in females. It is argued that bycatch in the Greenland halibut Reinhardtius hippoglossoides fishery has contributed to the observed shift, but also emphasised that such a distinct change could have a methodological component as well as being subject to effects of environmental change.

Field metabolic rates of teleost fishes are recorded in otolith carbonate.

Field metabolic rate (FMR) is key to understanding individual and population-level responses to environmental changes, but is challenging to measure in field conditions, particularly in aquatic environments. Here we show that FMR can be estimated directly from the isotopic composition of carbon in fish otoliths (δ13Coto). We describe the relationship between δ13Coto values and oxygen consumption rate, and report results from laboratory experiments relating individual-level measurements of oxygen consumption rates to δ13Coto values in Atlantic cod (Gadus morhua). We apply our new δ13Coto metabolic proxy to existing δ13Coto data from wild cod and four deepwater fish species to test the validity of inferred FMR estimates. The δ13Coto metabolic proxy offers a new approach to study physiological ecology in free-ranging wild fishes. Otolith-based proxies for FMR are particularly promising as they allow retrospective assessment of time-integrated, individual-level FMR throughout an individual fish's life history.

Stable coexistence of genetically divergent Atlantic cod ecotypes at multiple spatial scales.

Coexistence in the same habitat of closely related yet genetically different populations is a phenomenon that challenges our understanding of local population structure and adaptation. Identifying the underlying mechanisms for such coexistence can yield new insight into adaptive evolution, diversification and the potential for organisms to adapt and persist in response to a changing environment. Recent studies have documented cryptic, sympatric populations of Atlantic cod (Gadus morhua) in coastal areas. We analysed genetic origin of 6,483 individual cod sampled annually over 14 years from 125 locations along the Norwegian Skagerrak coast and document stable coexistence of two genetically divergent Atlantic cod ecotypes throughout the study area and study period. A "fjord" ecotype dominated in numbers deep inside fjords while a "North Sea" ecotype was the only type found in offshore North Sea. Both ecotypes coexisted in similar proportions throughout coastal habitats at all spatial scales. The size-at-age of the North Sea ecotype on average exceeded that of the fjord ecotype by 20% in length and 80% in weight across all habitats. Different growth and size among individuals of the two types might be one of several ecologically significant variables that allow for stable coexistence of closely related populations within the same habitat. Management plans, biodiversity initiatives and other mitigation strategies that do not account for the mixture of species ecotypes are unlikely to meet objectives related to the sustainability of fish and fisheries.

Genomic parallelism and lack thereof in contrasting systems of three-spined sticklebacks.

Parallel evolution and the extent to which it involves gene reuse have attracted much interest. Whereas it has theoretically been predicted under which circumstances gene reuse is expected, empirical studies that directly compare systems showing high and low parallelism are rare. Three-spined stickleback (Gasterosteus aculeatus), where freshwater populations have been independently founded by ancestral marine populations, represent prime examples of phenotypic and genomic parallelism, but cases exist where parallelism is low. Based on RAD (restriction site associated DNA) sequencing, we analysed SNPs and chromosome inversions in populations in Denmark and Greenland showing low and high parallelism, respectively. We identified parallelism across freshwater populations in Greenland at genomic regions previously identified to be associated with marine-freshwater divergence. These same markers also separated Danish marine and freshwater sticklebacks, albeit to a weaker extent. Hence, parallelism was not absent in Denmark but possibly constrained by spatially and temporally varying selection. Divergence time estimates found one Danish freshwater population to be much older than the others. It also deviated strongly with respect to parallelism and may represent earlier postglacial colonization based on a different pool of standing variation and eliciting different adaptive responses to freshwater conditions. These findings provide empirical support to previous suggestions that the time since replicate populations had access to a common pool of standing variation is a major factor determining gene reuse. At last, based on the observed parallelism in the Greenlandic system we discuss the predictability of adaptive responses in newly established populations.

Historical DNA documents long-distance natal homing in marine fish.

The occurrence of natal homing in marine fish remains a fundamental question in fish ecology as its unequivocal demonstration requires tracking of individuals from fertilization to reproduction. Here, we provide evidence of long-distance natal homing (>1000 km) over more than 60 years in Atlantic cod (Gadus morhua), through genetic analysis of archived samples from marked and recaptured individuals. Using a high differentiation single-nucleotide polymorphism assay, we demonstrate that the vast majority of cod tagged in West Greenland and recaptured on Icelandic spawning grounds belonged to the Iceland offshore population, strongly supporting a hypothesis of homing. The high degree of natal fidelity observed provides the evolutionary settings for development of locally adapted populations in marine fish and emphasize the need to consider portfolio effects in marine fisheries management strategies.

Archived DNA reveals fisheries and climate induced collapse of a major fishery.

Fishing and climate change impact the demography of marine fishes, but it is generally ignored that many species are made up of genetically distinct locally adapted populations that may show idiosyncratic responses to environmental and anthropogenic pressures. Here, we track 80 years of Atlantic cod (Gadus morhua) population dynamics in West Greenland using DNA from archived otoliths in combination with fish population and niche based modeling. We document how the interacting effects of climate change and high fishing pressure lead to dramatic spatiotemporal changes in the proportions and abundance of different genetic populations, and eventually drove the cod fishery to a collapse in the early 1970s. Our results highlight the relevance of fisheries management at the level of genetic populations under future scenarios of climate change.

A foraging cost of migration for a partially migratory cyprinid fish.

Migration has evolved as a strategy to maximise individual fitness in response to seasonally changing ecological and environmental conditions. However, migration can also incur costs, and quantifying these costs can provide important clues to the ultimate ecological forces that underpin migratory behaviour. A key emerging model to explain migration in many systems posits that migration is driven by seasonal changes to a predation/growth potential (p/g) trade-off that a wide range of animals face. In this study we assess a key assumption of this model for a common cyprinid partial migrant, the roach Rutilus rutilus, which migrates from shallow lakes to streams during winter. By sampling fish from stream and lake habitats in the autumn and spring and measuring their stomach fullness and diet composition, we tested if migrating roach pay a cost of reduced foraging when migrating. Resident fish had fuller stomachs containing more high quality prey items than migrant fish. Hence, we document a feeding cost to migration in roach, which adds additional support for the validity of the p/g model of migration in freshwater systems.

Adaptive differences in gene expression in European flounder (Platichthys flesus).

Population structure was previously believed to be very limited or absent in classical marine fishes, but recently, evidence of weakly differentiated local populations has been accumulating using noncoding microsatellite markers. However, the evolutionary significance of such minute genetic differences remains unknown. Therefore, in order to elucidate the relationship between genetic markers and adaptive divergence among populations of marine fishes, we combined cDNA microarray and microsatellite analysis in European flounders (Platichthys flesus). We demonstrate that despite extremely low levels of neutral genetic divergence, a high number of genes were significantly differentially expressed between North Sea and Baltic Sea flounders maintained in a long-term reciprocal transplantation experiment mimicking natural salinities. Several of the differentially regulated genes could be directly linked to fitness traits. These findings demonstrate that flounders, despite little neutral genetic divergence between populations, are differently adapted to local environmental conditions and imply that adaptation in gene expression could be common in other marine organisms with similar low levels of population subdivision.

Evolutionary mechanisms shaping the genetic population structure of marine fishes; lessons from the European flounder (Platichthys flesus L.).

A number of evolutionary mechanisms have been suggested for generating low but significant genetic structuring among marine fish populations. We used nine microsatellite loci and recently developed methods in landscape genetics and coalescence-based estimation of historical gene flow and effective population sizes to assess temporal and spatial dynamics of the population structure in European flounder (Platichthys flesus L.). We collected 1062 flounders from 13 localities in the northeast Atlantic and Baltic Seas and found temporally stable and highly significant genetic differentiation among samples covering a large part of the species' range (global F(ST) = 0.024, P < 0.0001). In addition to historical processes, a number of contemporary acting evolutionary mechanisms were associated with genetic structuring. Physical forces, such as oceanographic and bathymetric barriers, were most likely related with the extreme isolation of the island population at the Faroe Islands. A sharp genetic break was associated with a change in life history from pelagic to benthic spawners in the Baltic Sea. Partial Mantel tests showed that geographical distance per se was not related with genetic structuring among Atlantic and western Baltic Sea samples. Alternative factors, such as dispersal potential and/or environmental gradients, could be important for generating genetic divergence in this region. The results show that the magnitude and scale of structuring generated by a specific mechanism depend critically on its interplay with other evolutionary mechanisms, highlighting the importance of investigating species with wide geographical and ecological distributions to increase our understanding of evolution in the marine environment.

Long-term stability and effective population size in North Sea and Baltic Sea cod (Gadus morhua).

DNA from archived otoliths was used to explore the temporal stability of the genetic composition of two cod populations, the Moray Firth (North Sea) sampled in 1965 and 2002, and the Bornholm Basin (Baltic Sea) sampled in 1928 and 1997. We found no significant changes in the allele frequencies for the Moray Firth population, while subtle but significant genetic changes over time were detected for the Bornholm Basin population. Estimates of the effective population size (Ne) generally exceeded 500 for both populations when employing a number of varieties of the temporal genetic method. However, confidence intervals were very wide and Ne's most likely range in the thousands. There was no apparent loss of genetic variability and no evidence of a genetic bottleneck for either of the populations. Calculations of the expected levels of genetic variability under different scenarios of Ne showed that the number of alleles commonly reported at microsatellite loci in Atlantic cod is best explained by Ne's exceeding thousand. Recent fishery-induced bottlenecks can, however, not be ruled out as an explanation for the apparent discrepancy between high levels of variability and recently reported estimates of Ne << 1000. From life history traits and estimates of survival rates in the wild, we evaluate the compatibility of the species' biology and extremely low Ne/N ratios. Our data suggest that very small Ne's are not likely to be of general concern for cod populations and, accordingly, most populations do not face any severe threat of losing evolutionary potential due to genetic drift.

Evidence of a hybrid-zone in Atlantic cod (Gadus morhua) in the Baltic and the Danish Belt Sea revealed by individual admixture analysis.

The study of hybrid zones is central to our understanding of the genetic basis of reproductive isolation and speciation, yet very little is known about the extent and significance of hybrid zones in marine fishes. We examined the population structure of cod in the transition area between the North Sea and the Baltic Sea employing nine microsatellite loci. Genetic differentiation between the North Sea sample and the rest increased along a transect to the Baltic proper, with a large increase in level of differentiation occurring in the Western Baltic area. Our objective was to determine whether this pattern was caused purely by varying degrees of mechanical mixing of North Sea and Baltic Sea cod or by interbreeding and formation of a hybrid swarm. Simulation studies revealed that traditional Hardy-Weinberg analysis did not have sufficient power for detection of a Wahlund effect. However, using a model-based clustering method for individual admixture analysis, we were able to demonstrate the existence of intermediate genotypes in all samples from the transition area. Accordingly, our data were explained best by a model of a hybrid swarm flanked by pure nonadmixed populations in the North Sea and the Baltic Sea proper. Significant correlation of gene identities across loci (gametic phase disequilibrium) was found only in a sample from the Western Baltic, suggesting this area as the centre of the apparent hybrid zone. A hybrid zone for cod in the ecotone between the high-saline North Sea and the low-saline Baltic Sea is discussed in relation to its possible origin and maintenance, and in relation to a classical study of haemoglobin variation in cod from the Baltic Sea/Danish Belt Sea, suggesting mixing of two divergent populations without interbreeding.