Hybridization between genetically modified Atlantic salmon and wild brown trout reveals novel ecological interactions
- Proceedings. Biological sciences / The Royal Society
- Published almost 8 years ago
Interspecific hybridization is a route for transgenes from genetically modified (GM) animals to invade wild populations, yet the ecological effects and potential risks that may emerge from such hybridization are unknown. Through experimental crosses, we demonstrate transmission of a growth hormone transgene via hybridization between a candidate for commercial aquaculture production, GM Atlantic salmon (Salmo salar) and closely related wild brown trout (Salmo trutta). Transgenic hybrids were viable and grew more rapidly than transgenic salmon and other non-transgenic crosses in hatchery-like conditions. In stream mesocosms designed to more closely emulate natural conditions, transgenic hybrids appeared to express competitive dominance and suppressed the growth of transgenic and non-transgenic (wild-type) salmon by 82 and 54 per cent, respectively. To the best of our knowledge, this is the first demonstration of environmental impacts of hybridization between a GM animal and a closely related species. These results provide empirical evidence of the first steps towards introgression of foreign transgenes into the genomes of new species and contribute to the growing evidence that transgenic animals have complex and context-specific interactions with wild populations. We suggest that interspecific hybridization be explicitly considered when assessing the environmental consequences should transgenic animals escape to nature.
Gill disease in salmonids is characterized by a multifactorial aetiology. Epitheliocystis of the gill lamellae caused by obligate intracellular bacteria of the order Chlamydiales is one known factor; however, their diversity has greatly complicated analyses to establish a causal relationship. In addition, tracing infections to a potential environmental source is currently impossible. In this study, we address these questions by investigating a wild brown trout (Salmo trutta) population from seven different sites within a Swiss river system. One age class of fish was followed over 18 months. Epitheliocystis occurred in a site-specific pattern, associated with peak water temperatures during summer months. No evidence of a persistent infection was found within the brown trout population, implying an as yet unknown environmental source. For the first time, we detected ‘Candidatus Piscichlamydia salmonis’ and ‘Candidatus Clavochlamydia salmonicola’ infections in the same salmonid population, including dual infections within the same fish. These organisms are strongly implicated in gill disease of caged Atlantic salmon in Norway and Ireland. The absence of aquaculture production within this river system and the distance from the sea, suggests a freshwater origin for both these bacteria and offers new possibilities to explore their ecology free from aquaculture influences.
Anadromous and non-anadromous Arctic charr (Salvelinus alpinus) from multiple sample sites in Labrador, Canada were used to investigate possible differences in total mercury concentration ([THg]) between 1977-78 and 2007-09. The mean [THg] of anadromous Arctic charr was 0.03μg/g wet weight (ww) in 1977-78 and 0.04μg/g ww in 2007-09, while mean concentrations in non-anadromous conspecifics were 0.18μg/g ww in 1977-78 and 0.14μg/g ww in 2007-09. After correcting for the effects of fish age and fork-length, there was no widespread difference in the mean [THg] of anadromous or non-anadromous fish between the two time periods. However, at individual sites sampled during both time periods, [THg] increased, decreased, or did not change. The mean age of sampled fish declined from 9.0years in 1977-78 to 8.2years in 2007-09 for anadromous fish, and from 11.7years to 10.5years in non-anadromous Arctic charr. Similarly, mean fork-lengths decreased from 450mm to 417mm in anadromous and from 402mm to 335mm in non-anadromous fish between 1977-78 and 2007-09. The mean annual temperature at four Labrador weather stations increased by 1.6°C to 2.9°C between the two sampling periods. The lack of an overall trend in anadromous or non-anadromous Arctic charr [THg] despite warming temperatures that favour increased mercury methylation suggests that regional changes in climate-driven factors have had limited impacts on mercury exposure in Labrador freshwater or marine fish.
Temperature and egg viability data from an Arctic charr Salvelinus alpinus hatchery covering a period of 28 years were analysed. During the study period, there was a significant increase in the mean water temperature in May, July, August and September of c. 2° C. Independent of year, the egg viability showed a negative correlation with the mean monthly temperatures in July, August and September as well as with the temperature difference between October and November. The negative effect of high summer temperatures was further supported by a comparison of egg viability from replicate broodstock reared at two sites differing mainly in summer water temperature. The eggs from the colder site were, on average, significantly larger (4·4 mm compared with 4·0 mm) and had higher hatching rates (57% compared with 37%). These results suggest that unfavourable temperature conditions during the summer and autumn can explain much of the excessive egg mortality experienced at the main facility used for the Swedish S. alpinus breeding programme. The main effect was supra-optimal temperatures during the period July to September, but there also appears to have been an effect from the temperature regime before and during spawning (October to November) that was unrelated to the summer temperatures. These findings emphasize the importance of site selection and sustainable management of aquaculture hatcheries in the light of the ongoing climate change.
Land use and climate change occur simultaneously around the globe. Fully understanding their separate and combined effects requires a mechanistic understanding at the local scale where their effects are ultimately realized. Here we applied an individual-based model of fish population dynamics to evaluate the role of local stream variability in modifying responses of Coastal Cutthroat Trout (Oncorhynchus clarkii clarkii) to scenarios simulating identical changes in temperature and stream flows linked to forest harvest, climate change, and their combined effects over six decades. We parameterized the model for four neighboring streams located in a forested headwater catchment in northwestern Oregon, USA with multi-year, daily measurements of stream temperature, flow, and turbidity (2007-2011), and field measurements of both instream habitat structure and three years of annual trout population estimates. Model simulations revealed that variability in habitat conditions among streams (depth, available habitat) mediated the effects of forest harvest and climate change. Net effects for most simulated trout responses were different from or less than the sum of their separate scenarios. In some cases, forest harvest countered the effects of climate change through increased summer flow. Climate change most strongly influenced trout (earlier fry emergence, reductions in biomass of older trout, increased biomass of young-of-year), but these changes did not consistently translate into reductions in biomass over time. Forest harvest, in contrast, produced fewer and less consistent responses in trout. Earlier fry emergence driven by climate change was the most consistent simulated response, whereas survival, growth, and biomass were inconsistent. Overall our findings indicate a host of local processes can strongly influence how populations respond to broad scale effects of land use and climate change.
The parasitic salmon louse, and its resistance to chemical delousing agents, represents one of the largest challenges to the salmon aquaculture industry. We genotyped lice sampled from wild salmon and sea trout throughout Norway with the recently identified Phe362Tyr mutation that conveys resistance to organophosphates. These results were compared to data from lice sampled on farmed salmon in the same regions. The resistant ® allele was observed in salmon lice from wild salmon and sea trout throughout Norway, although its frequency was highest in farming-intense regions. In most regions, the frequency of the R allele was higher in lice collected from wild sea trout than wild Atlantic salmon, and in all regions, the frequency of the R allele was similar in lice collected from wild sea trout and farmed Atlantic salmon. The R allele is only selected for in fish-farms where organophosphates are used for delousing. Therefore, our results suggest extensive exchange of lice between farmed and wild hosts, and indicate that in farming-dense regions in Norway, aquaculture represents a major driver of salmon louse population structure. Finally, these data suggest that the wild hosts within the regions studied will not delay the spread of resistance when organophosphates are used.
We conducted a large-scale assessment of unconventional oil and gas (UOG) development effects on brook trout (Salvelinus fontinalis) distribution. We compiled 2231 brook trout collection records from the Upper Susquehanna River Watershed, USA. We used boosted regression tree (BRT) analysis to predict occurrence probability at the 1:24,000 stream-segment scale as a function of natural and anthropogenic landscape and climatic attributes. We then evaluated the importance of landscape context (i.e., pre-existing natural habitat quality and anthropogenic degradation) in modulating the effects of UOG on brook trout distribution under UOG development scenarios. BRT made use of 5 anthropogenic (28% relative influence) and 7 natural (72% relative influence) variables to model occurrence with a high degree of accuracy [Area Under the Receiver Operating Curve (AUC)=0.85 and cross-validated AUC=0.81]. UOG development impacted 11% (n=2784) of streams and resulted in a loss of predicted occurrence in 126 (4%). Most streams impacted by UOG had unsuitable underlying natural habitat quality (n=1220; 44%). Brook trout were predicted to be absent from an additional 26% (n=733) of streams due to pre-existing non-UOG land uses (i.e., agriculture, residential and commercial development, or historic mining). Streams with a predicted and observed (via existing pre- and post-disturbance fish sampling records) loss of occurrence due to UOG tended to have intermediate natural habitat quality and/or intermediate levels of non-UOG stress. Simulated development of permitted but undeveloped UOG wells (n=943) resulted in a loss of predicted occurrence in 27 additional streams. Loss of occurrence was strongly dependent upon landscape context, suggesting effects of current and future UOG development are likely most relevant in streams near the probability threshold due to pre-existing habitat degradation.
Salmonids are native from the North Hemisphere but have been introduced for aquaculture and sport fishing in the South Hemisphere and inhabit most rivers and lakes in temperate and cold regions worldwide. Five species are included in the Global Invasive Species Database: rainbow trout Oncorhynchus mykiss, Atlantic salmon Salmo salar, brown trout Salmo trutta, brook trout Salvelinus fontinalis, and lake trout Salvelinus namaycush. In contrast, other salmonids are endangered in their native settings.
Aquaculture production has nearly tripled in the last two decades, bringing with it a significant increase in the use of antibiotics. Using liquid chromatography/tandem mass spectrometry (LC-MS/MS), the presence of 47 antibiotics was investigated in U.S. purchased shrimp, salmon, catfish, trout, tilapia, and swai originating from 11 different countries. All samples (n=27) complied with U.S. FDA regulations and five antibiotics were detected above the limits of detection: oxytetracycline (in wild shrimp, 7.7ng/g of fresh weight; farmed tilapia, 2.7; farmed salmon, 8.6; farmed trout with spinal deformities, 3.9), 4-epioxytetracycline (farmed salmon, 4.1), sulfadimethoxine (farmed shrimp, 0.3), ormetoprim (farmed salmon, 0.5), and virginiamycin (farmed salmon marketed as antibiotic-free, 5.2). A literature review showed that sub-regulatory levels of antibiotics, as found here, can promote resistance development; publications linking aquaculture to this have increased more than 8-fold from 1991 to 2013. Although this study was limited in size and employed sample pooling, it represents the largest reconnaissance of antibiotics in U.S. seafood to date, providing data on previously unmonitored antibiotics and on farmed trout with spinal deformities. Results indicate low levels of antibiotic residues and general compliance with U.S. regulations. The potential for development of microbial drug resistance was identified as a key concern and research priority.
Different pathways of propagation and dispersal of non-native species into new environments may have contrasting demographic and genetic impacts on established populations. Repeated introductions of rainbow trout (Oncorhynchus mykiss) to Chile in South America, initially through stocking and later through aquaculture escapes, provide a unique setting to contrast these two pathways. Using a panel of single nucleotide polymorphisms, we found contrasting genetic metrics and patterns among naturalized trout in Lake Llanquihue, Chile’s largest producer of salmonid smolts for nearly 50 years, and Lake Todos Los Santos (TLS), a reference lake where aquaculture has been prohibited by law. Trout from Lake Llanquihue showed higher genetic diversity, weaker genetic structure, and larger estimates for the effective number of breeders (Nb) than trout from Lake TLS. Trout from Lake TLS were divergent from Lake Llanquihue and showed marked genetic structure and a significant isolation-by-distance pattern consistent with secondary contact between documented and undocumented stocking events in opposite shores of the lake. Multiple factors, including differences in propagule pressure, origin of donor populations, lake geomorphology, habitat quality or quantity, and life history, may help explain contrasting genetic metrics and patterns for trout between lakes. We contend that high propagule pressure from aquaculture may not only increase genetic diversity and Nb via demographic effects and admixture, but also may impact the evolution of genetic structure and increase gene flow, consistent with findings from artificially propagated salmonid populations in their native and naturalized ranges.