Retention of a chromosomal inversion from an anadromous ancestor provides the genetic basis for alternative freshwater ecotypes in rainbow trout

Migratory behaviour patterns in animals are controlled by a complex genetic architecture. Rainbow trout (Oncorhynchus mykiss) is a salmonid fish that spawns in streams but exhibits three primary life history pathways: stream‐resident (fluvial), lake‐migrant (adfluvial) and ocean‐migrant (anadromous). Previous studies examining fluvial and anadromous O. mykiss have identified several genes associated with life history divergence including the presence of an inversion complex within chromosome 5 (Omy05) that appears to maintain a suite of linked genes controlling migratory behaviour. However, adfluvial trout are migratory without being anadromous, and the genetic basis for this life history has not been investigated from evolutionary perspectives. We sampled wild, native nonanadromous rainbow trout occupying connected stream and lake habitats in a southwest Alaskan watershed to determine whether these fish exhibit genetic divergence between fluvial and adfluvial ecotypes, and whether that divergence parallels that documented in fluvial and anadromous O. mykiss. Data from restriction site‐associated DNA (RAD) sequencing revealed an association between frequencies of both the Omy05 inversion complex and other single nucleotide polymorphisms (SNPs) with habitat type (stream or lake), supporting the genetic divergence of fluvial and adfluvial individuals in sympatry. The presence of a genetic basis for migration into lakes, analogous to that documented for anadromy, indicates that the adfluvial ecotype must be recognized separately from the fluvial form of O. mykiss even though neither is anadromous. These results highlight the genetic architecture underlying migration and the importance of chromosomal inversions in promoting and sustaining intraspecific diversity.     

Differences in growth between offspring of anadromous and freshwater brown trout Salmo trutta

In this study, individual growth of juvenile offspring of anadromous and freshwater resident brown trout Salmo trutta and crosses between the two from the River Imsa, Norway, was estimated. The juveniles were incubated until hatching at two temperatures (±S.D. ), either 4.4 ± 1.5°C or 7.1 ± 0.6°C. Growth rate was estimated for 22 days in August–September when the fish on average were c. 8 g in wet mass, and the estimates were standardized to 1 g fish dry mass. Offspring of anadromous S. trutta grew better at both 15 and 18°C than offspring of freshwater resident S. trutta or offspring of crosses between the two S. trutta types. This difference appears not to result from a maternal effect because anadromous S. trutta grew better than the hybrids with anadromous mothers. Instead, this appears to be an inherited difference between the anadromous and the freshwater resident fish lending support to the hypothesis that anadromous and freshwater resident S. trutta in this river differ in genetic expression. Egg incubation temperature of S. trutta appeared not to influence the later growth as reported earlier from the studies of Atlantic salmon Salmo salar.     

Life history and genetic characterisation of sea trout Salmo trutta in the Adriatic Sea

1. The brown trout Salmo trutta is characterised by both anadromous (sea trout) and resident populations, naturally occurring in Atlantic and Ponto-Caspian rivers. Sea trout are currently considered absent from rivers of the Mediterranean area, probably because of the non-optimal chemical–physical characteristics of the Mediterranean Sea. However, the occasional bycatch of smoltified S. trutta in the Adriatic Sea is well known among fishermen and the biological explanation of this phenomenon is still controversial. The aim of this study was to compare the genetic diversity of freshwater and marine brown trout to try to understand the factors underlying the presence of putative anadromous brown trout in the Adriatic Sea.
2. In this study, we analysed the genetic diversity of: (1) wild brown trout collected from the Esino River (central Italy); (2) a domestic strain of brown trout used for stocking the study area; and (3) a sample of Adriatic sea trout collected near the outlet of the Esino River. Together with genetic analysis, we carried out scale analysis in order to track the freshwater/marine stages of the life cycle in the sea trout samples. The genetic characterisation was carried out by polymerase chain reaction–restriction fragment length polymorphism analysis of the mtDNA fragment ND-5/6 and the nuclear locus LDH-C1* and by genotyping 15 microsatellite loci. The genetic polymorphism obtained was used to investigate intra- and inter-population genetic diversity, rates of genetic introgression between wild and domestic samples and the origin of sea trout specimens by using assignment tests.
3. Our genetic analyses demonstrated that the sea trout analysed in this study are from the domestic strain of Atlantic origin used in central Italy for stocking activities. The level of genetic introgression between native and domestic samples is high in the Esino River. The populations more resilient to introgressive hybridisation appeared to be those living in the portion of the river network dominated by carbonate rocks. Assignment tests (GeneClass) suggest the existence of a link between stocking efforts and the freshwater origin of the sea trout. In addition, data obtained from the analysis of scales, size measurement, and sex determination showed a pattern of smolt age, size, and sex ratio very similar to those observed in other anadromous populations.
4. In conclusion, the present study highlighted that sea trout from the central Adriatic Sea originated from brown trout of Atlantic origin inhabiting the Esino River. Their seaward migratory behaviour could represent a consequence of an active migration instead of a passive displacement by water flow. Our results also showed that traditional stocking practices represent a negative activity for the conservation of the last Mediterranean native S. trutta populations.

     

Quantifying an overlooked aspect of partial migration using otolith microchemistry

For the first time, an overlooked aspect of partial migration was quantified using otolith microchemistry and brown trout, Salmo trutta, as a model species. Relative contributions of freshwater resident and anadromous female brown trout to mixed-stock sea trout populations in the Baltic Sea were estimated. Out of 236 confirmed wild sea trout sampled around the coast of Estonia 88% were of anadromous maternal origin and 12% were of resident maternal origin. This novel finding underscores the importance of the resident contingent in maintaining the persistence and resilience of the migratory contingent.     

Landscape features along migratory routes influence adaptive genomic variation in anadromous steelhead (Oncorhynchus mykiss)

Organisms typically show evidence of adaptation to features within their local environment. However, many species undergo long‐distance dispersal or migration across larger geographic regions that consist of highly heterogeneous habitats. Therefore, selection may influence adaptive genetic variation associated with landscape features at residing sites and along migration routes in migratory species. We tested for genomic adaptation to landscape features at natal spawning sites and along migration paths to the ocean of anadromous steelhead trout (Oncorhynchus mykiss) in the Columbia River Basin. Results from multivariate ordination, gene–environment association and outlier analyses using 24,526 single nucleotide polymorphisms (SNPs) provided evidence that adaptive allele frequencies were more commonly associated with landscape features along migration paths than features at natal sites (91.8% vs. 8.2% of adaptive loci, respectively). Among the 45 landscape variables tested, migration distance to the ocean and mean annual precipitation along migration paths were significantly associated with adaptive genetic variation in three distinct genetic groups. Additionally, variables such as minimum migration water temperature and mean migration slope were significant only in inland stocks of steelhead that migrate up to 1,200 km farther than those near the coast, indicating regional differences in migratory selective pressures. This study provides novel approaches for investigating migratory corridors and some of the first evidence that environment along migration paths can lead to substantial divergent selection. Consequently, our approach to understand genetic adaptation to migration conditions can be applied to other migratory species when migration or dispersal paths are generally known.     

Identifying sea-run brown trout, Salmo trutta, using Sr : Ca ratios of otolith

 The migratory history of the brown trout, Salmo trutta, collected from Japanese rivers, was examined in terms of strontium (Sr) and calcium (Ca) uptake in the otolith, by means of wavelength dispersive X-ray spectrometry on an electron microprobe. Sea-run (anadromous) and freshwater-resident (nonanadromous) types of S. trutta were found to occur sympatrically. Otolith Sr concentration or Sr : Ca ratios of anadromous S. trutta fluctuated strongly along the life history transect in accordance with the migration (habitat) pattern from sea to freshwater. In contrast, the Sr concentration or the Sr : Ca ratios of nonanadromous fish remained at consistently low levels throughout the otolith. The higher ratios in anadromous S. trutta, in the otolith region from the core to 1500 μm, corresponded to the initial seagoing period, probably reflecting the ambient salinity or the seawater–freshwater gradient in Sr concentration. The findings clearly indicated that otolith Sr : Ca ratios reflected individual life histories, enabling the sea-run S. trutta to be distinguished from the freshwater-resident brown trout. Received: March 18, 2002 / Revised: May 15, 2002 / Accepted: June 5, 2002 Acknowledgments The authors are grateful to Messrs. T. Ikeda, S. Kudo, Y. Miyakoshi, M. Nagata, K. Shimoda, T. Takami, K. Takeuchi, and M. Ueda for their assistance in collecting specimens. This work was supported in part by Grant-in-Aid No. 13760138 from the Ministry of Education, Culture, Sports, Science and Technology, Japan. Correspondence to:Takaomi Arai     

Riverine and near coastal migration performance of hatchery brown trout Salmo trutta

To study migration performance and return rates of hatchery brown trout Salmo trutta smolts the first 5 months after release, 50 fish in each year (fork length, L_F, 158–288 mm) were in two subsequent years tagged with acoustic transmitters and recorded by automatic listening stations in the River Nidelva (central Norway), its estuary and in the marine environment. More than half of the smolts became anadromous migrants (52% in 2011 and 70% in 2012). The fish spent longer time in the estuary than in the marine environment and the results suggest that migratory behaviour of S. trutta smolts is not only restricted to be resident or anadrome–lacustrine, but that there is also an intermediary strategy of estuarine feeding. There were no differences in L_F or mass between groups of smolts with different migration patterns. Return rates from the sea within the first 5 months after release were in both years 16%. Median progression rate in the river was 0·090 L_F s^?1 but decreased significantly as the smolts entered the estuary (0·015 L_F s^?1). The long residential time in the estuary may increase the risk of negative effects of anthropogenic activities in estuaries, such as harbours and industrial development, and special attention should be given to evaluate effects of such activities.     

Anadromous red-spotted masu salmon (Oncorhynchus masou ishikawae), a southernmost sea-migration form of salmonid,displays low variation in both age at seaward migration and sea age

We examined variations in age at seaward migration and sea age for the anadromous form of red-spotted masu salmon (Oncorhynchus masou ishikawae) in two Japanese rivers. The anadromous form of red-spotted masu salmon expressed only two sea migration patterns in the two rivers: (a) the majority of the salmon (95%, n = 81) were of age-0, and age-1 migrants were rare (n = 4); and (b) all the salmon examined (n = 22) made a return migration within a year, with 23% of the salmon exhibiting potamodromy in the river. Owing to low variation in their sea migratory patterns, the anadromous form of red-spotted masu salmon is likely vulnerable to environmental fluctuations.     

Spatial and Temporal Relations between Fluvial and Allacustrine Yellowstone Cutthroat Trout, Oncorhynchus clarki bouvieri, Spawning in the Yellowstone River, Outlet Stream of Yellowstone Lake

Yellowstone cutthroat trout (YCT), Oncorhynchus clarki bouvieri, that spawn in the outlet of Yellowstone Lake show two potamodromous migration patterns, fluvial and allacustrine. The main purpose of this study was to determine whether those fluvial and allacustrine YCT represent reproductively isolated stocks. Redd surveys indicated spawning occurred during about 5 consecutive weeks between late May and mid-July 1993–1995. Lake fish (N=6), defined as radiotagged YCT that entered Yellowstone Lake after the spawning period (i.e. allacustrine pattern), were found in the river between the lake outlet (river kilometer [Rkm] 0) and Rkm 20.0 during spawning. Probable lake fish (N=28; tagged YCT that were last detected near the lake outlet) were found between Rkm 0 and Rkm 22.5 during spawning. River fish (N=4; tagged YCT that remained in the river when annual tracking concluded in fall, i.e. fluvial pattern) were found between Rkm 1.1 and Rkm 18.0 during spawning. Fidelity to spawning areas used between consecutive years was suggested by one of five lake fish and the single river fish for which data were available. Spatial overlap in spawning and a lack of temporal separation between the life-history types during spawning suggested that fluvial and allacustrine YCT were not reproductively isolated. Radiotagging, as well as visual observations made annually from boats during April and May, indicated fluvial YCT overwintered downstream from Rkm 14 and were few, probably on the order of 10% of all YCT that spawned in the Yellowstone River.     

Environmental signature in the otolith elemental fingerprint of the tapertail anchovy, Coilia mystus, from the Changjiang estuary, China

The ontogenetic patterns of habitat use and the migratory history of the tapertail anchovy, Coilia mystus, collected in the Changjiang estuary around Chongming Island, China, were studied by examining the environmental signature in the otolith strontium (Sr) and calcium (Ca) fingerprints using electron probe microanalysis (EPMA). Our results suggest that the migration strategy of C. mystus is much more flexible than supposed in the literature to date. The spring spawning population of C. mystus from the studied area was found to consist of individuals with different migration histories. Although the tapertail anchovy seems to be an anadromous fish that spawns and hatches in a freshwater habitat, it can also use a freshwater environment in non‐spawning seasons. The otolith EPMA of the elemental fingerprint (Sr x‐ray maps and Sr : Ca ratios) is an environmental indicator that can be applied to the migratory ecology of other important diadromous species in China.     

Does reduced feeding prior to release improve the marine migration of hatchery brown trout Salmo trutta smolts?

The aim of this study was to test the hypothesis that hatchery brown trout Salmo trutta smolts, with 50% reduced or no feeding over the last 5 months before release, were more likely to migrate to the sea than individuals with standard feeding ratios. The juvenile fish were divided into three groups 176 days before release: (A) with no feeding, (B) with 50% and (C) with 100% feeding. To study their seaward migration, 40 fish from each feeding group were tagged with acoustic transmitters and tracked by automatic listening stations in the River Nidelva, Trondheim, Norway, its estuary and in the nearest marine environment. At the time of release, mean condition factor was significantly lower in group A and the fish from groups A and B had higher levels of Na+, K+‐ATPase. Significantly more fish from group A migrated to the sea, but the rate of downstream progression from release to the estuary did not differ between the three groups. In conclusion, the S. trutta smolts with no access to food in the last 176 day before release were more likely to migrate to the sea. Fish from all three feeding groups, however, appeared to smoltify and had the same rate of downstream progression to the estuary. This indicates that differences in migratory behaviour between individuals from the three feeding groups begin from the time when the fish reach saline waters. It is suggested that feeding in hatcheries has to be greatly reduced (by 50% or more) over several months to have a pronounced effect on the migratory behaviour in S. trutta.     

Acoustic barriers as an acoustic deterrent for native potamodromous migratory fish species

This study focused on the use of sound playbacks as acoustic deterrents to direct native potamodromous migratory species away from all kind of traps. The effects of two acoustic treatments, a repeated sine sweep up to 2 kHz (sweep-up stimulus) and an intermittent 140 Hz tone, were tested in three fish species native to Iberia: Salmo trutta, Pseudochondrostoma duriense and Luciobarbus bocagei. In contrast with S. trutta, the endemic cyprinids P. duriense and L. bocagei exhibited a strong repulse reaction to the frequency sweep-up sound. The 140 Hz stimulus did not seem to alter significantly the behaviour of any of the studied species. These results highlight the potential of acoustic stimuli as fish behavioural barriers and their application to in situ conservation measures of native Iberian fish populations, to protect them from hydropower dams. In addition, this study shows that acoustic deterrents can be used selectively on target species.     

Maternal influence on early lipid content in an introduced partially anadromous population of Oncorhynchus mykiss

This study evaluated how the maternal migratory tactic in a partially anadromous population of Oncorhynchus mykiss may influence the early energetic status of their offspring. Total lipid content variation (% dry mass) of recently emerged fry caught in the Santa Cruz River, Argentina, was evaluated as a function of their maternal origin (anadromous v. resident) and fork length (L_F). Lipid content of fry decreased with L_F and was higher for offspring of anadromous mothers.     

Does the trace element composition of brown trout Salmo trutta eggs remain unchanged in spawning redds?

The temporal stability of trace element concentrations in fertilized, artificially incubated anadromous brown trout Salmo trutta eggs and newly hatched fry was investigated. The anadromous status of the parental fish was confirmed using strontium isotopic analysis of otoliths. Whilst manganese concentrations in eggs varied over time, concentrations of aluminium, potassium, magnesium, strontium, barium and calcium were all unchanged 1 week and 6 weeks post‐fertilization as well as in recently hatched larvae. The results clearly suggest that the distinctive trace element signature present in the eggs and newly hatched larvae of anadromous S. trutta (typically characterized by high strontium, low barium) is stable over time. Therefore analysis of the trace element composition of eggs is concluded to be a cost‐effective and reliable method for determining the spatial and temporal extent of upstream spawning migration by anadromous salmonids. The temporal variability of at least one element in this study suggests the stability of untested multi‐element signatures cannot automatically be assumed.     

Factors influencing return rate and marine residence duration in sea trout populations in Central Norway

Brown trout (Salmo trutta) display extensive plasticity in marine migratory behaviours, with marine migrations considered to be an adaptive strategy which enables sea trout to maximize growth and reproductive potential. However, marine migrations are not without associated costs, including threats posed by ever-increasing salmon lice (Lepeophtheirus salmonis) infestations. In the present study, we used passive integrated transponder technology to characterize variability in sea trout migration behaviour amongst three catchments situated in a region of intensive salmon farming in central Norway. Specifically, we investigate how lice infestation, out-migration date and body size alter sea trout return rate and marine residence duration during the first out-migration to sea from each catchment. Distinct catchment-specific differences in sea trout out-migration size and the number of cohorts were observed, but larger body size did not guarantee the successful return of migrating trout. The marine residence duration of individuals that successfully returned to freshwater was positively correlated with lice infestation risk, suggesting for these individuals the lethal infestation threshold had not been reached. Our results also suggest that sea trout populations from lotic-dominated catchments are potentially at greater risk from size-related threats to their survival encountered during their marine migrations than sea trout from lentic-dominated catchments. The variability in sea trout migratory behaviour amongst catchments observed here emphasizes the challenges fisheries managers face when deciding the best actions to take to protect the anadromous portion of brown trout populations.     

Impacts of acidification on brown trout Salmo trutta populations and the contribution of stocking to population recovery and genetic diversity

Anthropogenic acidification in SW-Scotland, from the early 19th Century onwards, led to the extinction of several loch (lake) brown trout (Salmo trutta) populations and substantial reductions in numbers in many others. Higher altitude populations with no stocking influence, which are isolated above natural and artificial barriers and subjected to the greatest effect of acidification, exhibited the least intrapopulation genetic diversity (34% of the allelic richness of the populations accessible to anadromous S. trutta). These, however, were characterised by the greatest interpopulation divergence (highest pairwise D_EST 0.61 and F_ST 0.53 in contemporary samples) based on 16 microsatellite loci and are among the most differentiated S. trutta populations in NW-Europe. Five lochs above impassable waterfalls, where S. trutta were thought to be extinct, are documented as having been stocked in the late 1980s or 1990s. All five lochs now support self-sustaining S. trutta populations; three as a direct result of restoration stocking and two adjoining lochs largely arising from a small remnant wild population in one, but with some stocking input. The genetically unique Loch Grannoch S. trutta, which has been shown to have a heritable increased tolerance to acid conditions, was successfully used as a donor stock to restore populations in two acidic lochs. Loch Fleet S. trutta, which were re-established from four separate donor sources in the late 1980s, showed differential contribution from these ancestors and a higher genetic diversity than all 17 natural loch populations examined in the area. Genetically distinct inlet and outlet spawning S. trutta populations were found in this loch. Three genetically distinct sympatric populations of S. trutta were identified in Loch Grannoch, most likely representing recruitment from the three main spawning rivers. A distinct genetic signature of Loch Leven S. trutta, the progenitor of many Scottish farm strains, facilitated detection of stocking with these strains. One artificially created loch was shown to have a population genetically very similar to Loch Leven S. trutta. In spite of recorded historical supplemental stocking with Loch Leven derived farm strains, much of the indigenous S. trutta genetic diversity in the area remains intact, aside from the effects of acidification induced bottlenecks. Overall genetic diversity and extant populations have been increased by allochthonous stocking.     

The role of <Emphasis Type="Italic">Dlx</Emphasis> homeogenes in early development of the olfactory pathway

Development of the olfactory pathway requires interaction between cells and signals of different origin. Olfactory receptor neurons (ORN) in the olfactory placodes (OP) extend axons towards the forebrain (FB); with innervation taking place at a later time following degradation of the basement membrane. Cells from the OP migrate along ORN axons and differentiate into various elements, including ensheathing and Gonadotropin Releasing Hormone (GnRH)+ cells. The importance of the olfactory connection and migration is highlighted by the severe endocrine phenotype in Kallmann’s patients who lack this migratory pathway. Little is known about the genetic control of intrinsic ORN properties. Inactivation of the distalless-related Dlx5 prevents connections between ORNs and FB. Using a grafting approach we show that misguidance and lack of connectivity is due to intrinsic defects in ORN neurites and migratory cells (MgC), and not to environmental factors. These data point to a cell-autonomous function of Dlx5 in providing ORN axons with their connectivity properties. Dlx5 also marks a population of early MgC that partly overlaps with the GnRH+ population. In the absence of Dlx5 MgCs of the Dlx5+ lineage migrate, associated with PSA-NCAM+ axons, but fail to reach the FB as a consequence of the lack of axonal connection and not an inability to migrate. These data suggests that Dlx5 is not required to initiate migration and differentiation of MgCs. An erratum to this article can be found at     

Mismatch between fishway operation and timing of fish movements: a risk for cascading effects in partial migration systems

Habitat fragmentation is a growing problem worldwide. Particularly in river systems, numerous dams and weirs hamper the movement of a wide variety of species. With the aim to preserve connectivity for fish, many barriers in river systems are equipped with fishways (also called fish passages or fish ladders). However, few fishways provide full connectivity. Here we hypothesized that restricted seasonal opening times of fishways can importantly reduce their effectiveness by interfering with the timing of fish migration, for both spring‐ and autumn‐spawning species. We empirically tested our hypothesis, and discuss the possible eco‐evolutionary consequences of affected migration timing. We analyzed movements of two salmonid fishes, spring‐spawning European grayling (Thymallus thymallus) and autumn‐spawning brown trout (Salmo trutta), in Norway's two largest river systems. We compared their timing of upstream passage through four fishways collected over 28 years with the timing of fish movements in unfragmented river sections as monitored by radiotelemetry. Confirming our hypothesis, late opening of fishways delayed the migration of European grayling in spring, and early closure of fishways blocked migration for brown trout on their way to spawning locations during late autumn. We show in a theoretical framework how restricted opening times of fishways can induce shifts from migratory to resident behavior in potamodromous partial migration systems, and propose that this can induce density‐dependent effects among fish accumulating in lower regions of rivers. Hence, fragmentation may not only directly affect the migratory individuals in the population, but may also have effects that cascade downstream and alter circumstances for resident fish. Fishway functionality is inadequate if there is a mismatch between natural fish movements and fishway opening times in the same river system, with ecological and possibly evolutionary consequences for fish populations.     

Long-term investigations of migratory behaviour of asp (Aspius aspius L.) in the middle part of the Elbe River, Germany

The migratory behaviour, habitat use, home range and temporal and spatial variability of migrations of the potamodromous asp (Aspius aspius L.) in the large Elbe River, Germany, were studied in the years 1997–2000. Fifty‐three asp were tagged with surgically implanted radio transmitters and individually hand‐tracked usually once per week for about 1 year; 50% of the asp exclusively inhabited the main channel, 22% moved for short visits into other habitats and 24% changed between winter habitats in a harbour or oxbow and summer habitats in the main channel where they spawned in late March/April. The migratory behaviour of asp was highly variable; 34 asp observed for more than 1 year lived in home ranges of 1 to >100 stream kilometres (skm) mostly near their capture site. Longest observed migration from summer habitat in the Tidal Elbe back to the spawning ground in the Middle Elbe was 166 skm. After the spawning period or the spawning period thereafter, nine of these 34 fish left their home ranges for a long downstream migration without returning during the observation period. From these results we conclude that populations of rheophilic, potamodromous fish use a surprisingly long river section and that weirs have a strong impact on migration patterns and, ultimately, on population dynamics of these species.