Migrating silver eels return from the sea to the river of origin after a false start

The European eel's singular spawning migration from European waters towards the Sargasso Sea remains elusive, including the early phase of migration at sea. During spawning migration, the movement of freshwater resident eels from river to sea has been thought to be irreversible. We report the first recorded incidents of eels returning to the river of origin after spending up to a year in the marine environment. After migrating to the Baltic Sea, 21% of the silver eels, tagged with acoustic transmitters, returned to the Narva River. Half returned 11–12 months after moving to the sea, with 15 km being the longest upstream movement. The returned eels spent up to 33 days in the river and migrated to the sea again. The fastest specimen migrated to the outlet of the Baltic Sea in 68 days after the second start—roughly 1300 km. The surprising occurrence of returning migrants has implications for sustainable management and protection of this critically endangered species.

Photoperiod-dependent developmental reprogramming of the transcriptional response to seawater entry in Atlantic salmon (Salmo salar)

The developmental transition of juvenile salmon from a freshwater resident morph (parr) to a seawater (SW) migratory morph (smolt), known as smoltification, entails a reorganization of gill function to cope with the altered water environment. Recently, we used RNAseq to characterize the breadth of transcriptional change which takes place in the gill in the FW phase of smoltification. This highlighted the importance of extended exposure to short, winter-like photoperiods (SP) followed by a subsequent increase in photoperiod for completion of transcriptional reprogramming in FW and for efficient growth following transfer to SW. Here, we extend this analysis to examine the consequences of this photoperiodic history-dependent reprogramming for subsequent gill responses upon exposure to SW. We use RNAseq to analyse gill samples taken from fish raised on the photoperiod regimes we used previously and then challenged by SW exposure for 24-h. While fish held on constant light (LL) throughout were able to hypo-osmoregulate during a 24-h SW challenge, the associated gill transcriptional response was highly distinctive from that in fish which had experienced an 7 week period of exposure to SP followed by a return to LL (SPLL) and had consequently acquired the characteristics of fully developed smolts. Fish transferred from LL to SP, and then held on SP for the remainder of the study were unable to hypo-osmoregulate, and the associated gill transcriptional response to SW exposure featured many transcripts apparently regulated by the glucocorticoid stress axis and by the osmo-sensing transcription factor NFAT5. The importance of these pathways for the gill transcriptional response to SW exposure appears to diminish as a consequence of photoperiod mediated induction of the smolt phenotype, presumably reflecting preparatory developmetal changes taking place during this process.

Genomic Architecture of Rapid Parallel Adaptation to Fresh Water in a Wild Fish

Rapid adaptation to novel environments may drive changes in genomic regions through natural selection. However, the genetic architecture underlying these adaptive changes is still poorly understood. Using population genomic approaches, we investigated the genomic architecture that underlies rapid parallel adaptation of Coilia nasus to fresh water by comparing four freshwater-resident populations with their ancestral anadromous population. Linkage disequilibrium network analysis and population genetic analyses revealed two putative large chromosome inversions on LG6 and LG22, which were enriched for outlier loci and exhibited parallel association with freshwater adaptation. Drastic frequency shifts and elevated genetic differentiation were observed for the two chromosome inversions among populations, suggesting that both inversions would undergo divergent selection between anadromous and resident ecotypes. Enrichment analysis of genes within chromosome inversions showed significant enrichment of genes involved in metabolic process, immunoregulation, growth, maturation, osmoregulation, and so forth, which probably underlay differences in morphology, physiology and behavior between the anadromous and freshwater-resident forms. The availability of beneficial standing genetic variation, large optimum shift between marine and freshwater habitats, and high efficiency of selection with large population size could lead to the observed rapid parallel adaptive genomic change. We propose that chromosomal inversions might have played an important role during the evolution of rapid parallel ecological divergence in the face of environmental heterogeneity in C. nasus. Our study provides insights into the genomic basis of rapid adaptation of complex traits in novel habitats and highlights the importance of structural genomic variants in analyses of ecological adaptation.

Photoperiod-dependent developmental reprogramming of the transcriptional response to seawater entry in Atlantic salmon (Salmo salar)

The developmental transition of juvenile salmon from a freshwater resident morph (parr) to a seawater (SW) migratory morph (smolt) requires a range of physiological adaptations, including the capacity to hypo-osmoregulate. This process, known as smolting, involves both photoperiod-dependent preparative changes before SW is encountered, and activational changes stimulated by exposure to SW. To explore the relationship between these two aspects we undertook experiments in which physiological and transcriptomic responses to SW-challenge were assessed in fish that had experienced different histories of photoperiodic exposure. Compared to fish held on constant light (LL), exposure to short photoperiod (SP) dramatically impaired hypo-osmoregulation in SW, and was associated with extensive glucocorticoid-related changes in gill gene expression. Additionally, a major effect of photoperiodic history was observed in the transcriptional response of LL-acclimated fish to SW, with the response profiles of fish held on LL throughout life being quite distinctive from those of fish which had experienced an 8 week period of exposure to SP prior to return to LL (SPLL). These differences in profile likely reflect a diminishing role for NFAT-mediated responses in SPLL fish, as pathways linked to acute changes in cellular tonicity or intracellular calcium levels decline in importance with preparation for SW.

Kokanee–sockeye salmon hybridization leads to intermediate morphology and resident life history: implications for fisheries management

Stocking programs designed to return extirpated species to their historical range have become increasingly prevalent, punctuating the need to better understand the risks posed to recipient ecosystems. Here, we investigated the genetic and biological consequences of an anadromous sockeye salmon (Oncorhynchus nerka) stocking program in Skaha Lake, British Columbia, where substantial levels of hybridization and introgression with the native freshwater resident ecotype (kokanee) have been detected. We genetically assigned 543 individuals (adult spawners, age-0 juveniles) to estimate stock proportions (pure-stock sockeye, pure-stock kokanee, or hybrid) between 2010 and 2017, with a subset undergoing otolith microchemistry analysis to determine migratory life history and maternal ancestry. The proportion of hybrid spawners varied from 5% to 20% across sampling years, while that of hybrid age-0 juveniles remained relatively constant (∼11%). Hybrid spawners exhibited intermediate size relative to pure stocks, with the vast majority being nonanadromous (92%) and of resident maternal ancestry (76%). Our results provide empirical support for previously hypothesized mechanisms of hybridization between O. nerka life-history forms and underscore the importance of continued monitoring of stocking programs to quantify long-term fitness impacts of introgression and refine management strategies.

Early growth, mortality, and partial migration of striped bass (Morone saxatilis) larvae and juveniles in the St. Lawrence estuary, Canada

After being extirpated from the St. Lawrence Estuary (SLE), striped bass (Morone saxatilis) were reintroduced in 2002, and by 2008 they were naturally reproducing. The increase of this reintroduced population prompted the need to document its nursery habitats utilization, which contribute to species recruitment. We analysed mortality-dispersion rates and the growth of larvae and juveniles in relation to their occurrence and migration patterns. From June to September 2014, we collected striped bass distributed in four estuarine habitats: the upstream freshwater section (UP), the oligohaline (O-ETM) and the mesohaline (M-ETM) estuarine turbidity maximum zone, and the downstream polyhaline section (DOWN). Based on otolith microstructure and microchemistry, 305 back-calculated growth and 36 migration trajectories have been reconstructed. The UP and the O-ETM provided optimal conditions wherein which larvae and juveniles exhibited fastest growth. In the SLE, we emphasized the co-existence of a freshwater resident contingent and two migrant contingents to the M-ETM and DOWN. We propose that migrants adopt an adaptive migration behaviour to avoid suboptimal conditions and strong intraspecific competition from resident in the upstream habitats. The potential advantage of a downstream migration later in the season might be an adaptative strategy to promote their survival during the early life stages.

Influence of parental life history on maturation and smoltification in brown trout (Salmo trutta L.)

The developmental pathways of the offspring of three groups of trout, Salmo trutta L., with known life histories were compared: one group from a freshwater resident population and two groups from an anadromous population (fish that have smoltified and fish that have not). The fish were hybridized within a group, and 27 families were obtained and reared mixed in two tanks. Tracking fish specimens was possible thanks to individual passive integrated transponder (PIT) tagging. All families followed different life pathways. Faster growth favored early smoltification and maturation at the age of 1+ in males that had not smoltified. In addition, both processes were clearly also influenced by inherited factors. Fish of freshwater resident origin smoltified more infrequently, and males matured earlier than did fish from the migratory population. The offspring of parents from the migratory population, which did smoltify during their individual histories, smoltified early (in the second year) more often than offspring of non-smoltified members of the population.