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Evaluation of a microsatellite panel for use across North American populations of white-tailed deer (Odocoileus virginianus)

Background Microsatellite loci have been used extensively over the past two decades to study the genetic characteristics of non-model species. The relative ease of microsatellite development and ability to adapt markers from related species has led to the proliferation of available markers, particularly for those species that are intensively studied and managed. Because it is often infeasible to genotype individuals across all available loci, researchers generally rely on subsets of markers. Marker choice and genotyping errors can bias inferences made using disparate suites of microsatellite loci. This can limit comparative and collaborative efforts among research groups and has been a primary motivation for panel standardization efforts. Here, we develop a methodology for identifying a suite of markers from previous literature that can be generalizable across the range of commonly studied organisms. We specifically focus on producing a broadly applicable microsatellite panel for white-tailed deer ( Odocoileus virginianus ). Results We reviewed microsatellite panels from 58 previous or ongoing projects and identified a total of 106 candidate loci. We developed a multiplex protocol and evaluated the efficacy of 17 of the most commonly used loci using 720 DNA samples collected from the Mid-Atlantic region of the United States, an area where few previous studies were conducted. Amplification errors were detected in six of these loci. The properties of the remaining 11 loci suggest that they are applicable for many common research objectives. Specifically, this panel is highly polymorphic (eight to 20 alleles per locus, polymorphic information criterion = 0.492 to 0.917), exhibits low frequencies of genotyping errors (null alleles < 10%), and is relatively easy to interpret with the aid of allele binning software. Conclusions We were able to identify a panel of microsatellite markers that show potential for broad applicability over the geographic range of white-tailed deer, as evidenced by the distribution of previous studies that utilized them. Validation in an additional region confirmed this. These results suggest that marker standardization and evaluation procedures based on literature reviews offers an effective method for identifying consolidated panels for future studies. This simple procedure addresses previous concerns about the infeasibility of standardization efforts.

Maryland, Pennsylvania, Virginia

Development of microsatellite markers for three at risk tiger beetles Cicindela dorsalis dorsalis, C. d. media, and C. puritana

Objective Tiger beetles inhabiting sandy beaches and cliffs along the east coast of the United States are facing increasing habitat loss due to erosion, urbanization, and sea level rise. The northeastern beach tiger beetle Cicindela dorsalis dorsalis and Puritan tiger beetle Cicindela puritana are both listed as threatened under the Endangered Species Act of 1973, while the white beach tiger beetle Cicindela dorsalis media is not listed but has been declining. Extirpation of these beetles, in some cases from entire states, has isolated many populations reducing gene flow and elevating the risk for the loss of genetic variation. To facilitate investigations of population genetic structure, we developed suites of microsatellite loci for conservation genetic studies. Results Shotgun genomic sequencing of all species identified thousands of candidate microsatellite loci, among which 17 loci were optimized and verified to cross-amplify within C. d. media and C. d. dorsalis , and eight separate loci were optimized for C. puritana . Most loci conformed to Hardy–Weinberg equilibrium, showed no evidence of linkage disequilibrium or null alleles, and revealed population genetic characteristics informative for natural resource managers among the populations tested.

BMC Research Notes

Microsatellite marker development from next-generation sequencing in the New England cottontail (Sylvilagus transitionalis) and cross-amplification in the eastern cottontail (S. floridanus)

Objective The New England cottontail ( Sylvilagus transitionalis ) is a species of high conservation priority in the Northeastern United States, and was a candidate for federal listing under the Endangered Species Act until a recent decision determined that conservation actions were sufficient to preclude listing. The aim of this study was to develop a suite of microsatellite loci to guide future research efforts such as the analysis of population genetic structure, genetic variation, dispersal, and genetic mark-recapture population estimation. Results Thirty-five microsatellite markers containing tri- and tetranucleotide sequences were developed from shotgun genomic sequencing of tissue from S. transitionalis , S. obscurus , and S. floridanus . These loci were screened in n = 33 wild S. transitionalis sampled from a population in eastern Massachusetts, USA. Thirty-two of the 35 loci were polymorphic with 2–6 alleles, and observed heterozygosities of 0.06–0.82. All loci conformed to Hardy–Weinberg Equilibrium proportions and there was no evidence of linkage disequilibrium or null alleles. Primers for 33 of the 35 loci amplified DNA extracted from n = 6 eastern cottontail ( S. floridanus ) samples, of which nine revealed putative species-diagnostic alleles. These loci will provide a useful tool for conservation genetics investigations of S. transitionalis and a potential diagnostic species assay for differentiating sympatric eastern and New England cottontails.

Massachusetts

An empirical comparison of population genetic analyses using microsatellite and SNP data for a species of conservation concern

Background Use of genomic tools to characterize wildlife populations has increased in recent years. In the past, genetic characterization has been accomplished with more traditional genetic tools (e.g., microsatellites). The explosion of genomic methods and the subsequent creation of large SNP datasets has led to the promise of increased precision in population genetic parameter estimates and identification of demographically and evolutionarily independent groups, as well as questions about the future usefulness of the more traditional genetic tools. At present, few empirical comparisons of population genetic parameters and clustering analyses performed with microsatellites and SNPs have been conducted. Results Here we used microsatellite and SNP data generated from Gunnison sage-grouse ( Centrocercus minimus ) samples to evaluate concordance of the results obtained from each dataset for common metrics of genetic diversity ( H O , H E , F IS , A R ) and differentiation ( F ST , G ST , D Jost ). Additionally, we evaluated clustering of individuals using putatively neutral (SNPs and microsatellites), putatively adaptive, and a combined dataset of putatively neutral and adaptive loci. We took particular interest in the conservation implications of any differences. Generally, we found high concordance between microsatellites and SNPs for H E , F IS , A R , and all differentiation estimates. Although there was strong correlation between metrics from SNPs and microsatellites, the magnitude of the diversity and differentiation metrics were quite different in some cases. Clustering analyses also showed similar patterns, though SNP data was able to cluster individuals into more distinct groups. Importantly, clustering analyses with SNP data suggest strong demographic independence among the six distinct populations of Gunnison sage-grouse with some indication of evolutionary independence in two or three populations; a finding that was not revealed by microsatellite data. Conclusion We demonstrate that SNPs have three main advantages over microsatellites: more precise estimates of population-level diversity, higher power to identify groups in clustering methods, and the ability to consider local adaptation. This study adds to a growing body of work comparing the use of SNPs and microsatellites to evaluate genetic diversity and differentiation for a species of conservation concern with relatively high population structure and using the most common method of obtaining SNP genotypes for non-model organisms.

Arizona, Colorado, New Mexico, Utah

Evidence that pairing with genetically similar mates is maladaptive in a monogamous bird

Background Evidence of multiple genetic criteria of mate choice is accumulating in numerous taxa. In many species, females have been shown to pair with genetically dissimilar mates or with extra-pair partners that are more genetically compatible than their social mates, thereby increasing their offsprings' heterozygosity which often correlates with offspring fitness. While most studies have focused on genetically promiscuous species, few studies have addressed genetically monogamous species, in which mate choice tends to be mutual. Results Here, we used microsatellite markers to assess individual global heterozygosity and genetic similarity of pairs in a socially and genetically monogamous seabird, the black-legged kittiwake Rissa tridactyla . We found that pairs were more genetically dissimilar than expected by chance. We also identified fitness costs of breeding with genetically similar partners: (i) genetic similarity of pairs was negatively correlated with the number of chicks hatched, and (ii) offspring heterozygosity was positively correlated with growth rate and survival. Conclusion These findings provide evidence that breeders in a genetically monogamous species may avoid the fitness costs of reproducing with a genetically similar mate. In such species that lack the opportunity to obtain extra-pair fertilizations, mate choice may therefore be under high selective pressure.

Alaska

Distribution and population genetics of walleye and sauger

Conserving genetic diversity and local adaptations are management priorities for wild populations of exploited species, which increasingly are subject to climate change, habitat loss, and pollution. These constitute growing concerns for the walleye Sander vitreus, an ecologically and economically valuable North American temperate fish with large Laurentian Great Lakes' fisheries. This study compares genetic diversity and divergence patterns across its widespread native range using mitochondrial (mt) DNA control region sequences and nine nuclear DNA microsatellite (μsat) loci, examining historic and contemporary influences. We analyze the genetic and morphological characters of a putative endemic variant– “blue pike” S. v. “glaucus” –described from Lakes Erie and Ontario, which became extinct. Walleye with turquoise-colored mucus also are evaluated, since some have questioned whether these are related to the “blue pike”.

BMC Evolutionary Biology

Genetic and phenotypic variation along an ecological gradient in lake trout Salvelinus namaycush

Background Adaptive radiation involving a colonizing phenotype that rapidly evolves into at least one other ecological variant, or ecotype, has been observed in a variety of freshwater fishes in post-glacial environments. However, few studies consider how phenotypic traits vary with regard to neutral genetic partitioning along ecological gradients. Here, we present the first detailed investigation of lake trout Salvelinus namaycush that considers variation as a cline rather than discriminatory among ecotypes. Genetic and phenotypic traits organized along common ecological gradients of water depth and geographic distance provide important insights into diversification processes in a lake with high levels of human disturbance from over-fishing. Results Four putative lake trout ecotypes could not be distinguished using population genetic methods, despite morphological differences. Neutral genetic partitioning in lake trout was stronger along a gradient of water depth, than by locality or ecotype. Contemporary genetic migration patterns were consistent with isolation-by-depth. Historical gene flow patterns indicated colonization from shallow to deep water. Comparison of phenotypic ( Pst ) and neutral genetic variation ( Fst ) revealed that morphological traits related to swimming performance (e.g., buoyancy, pelvic fin length) departed more strongly from neutral expectations along a depth gradient than craniofacial feeding traits. Elevated phenotypic variance with increasing water depth in pelvic fin length indicated possible ongoing character release and diversification. Finally, differences in early growth rate and asymptotic fish length across depth strata may be associated with limiting factors attributable to cold deep-water environments. Conclusion We provide evidence of reductions in gene flow and divergent natural selection associated with water depth in Lake Superior. Such information is relevant for documenting intraspecific biodiversity in the largest freshwater lake in the world for a species that recently lost considerable genetic diversity and is now in recovery. Unknown is whether observed patterns are a result of an early stage of incipient speciation, gene flow-selection equilibrium, or reverse speciation causing formerly divergent ecotypes to collapse into a single gene pool.

Lake Superior, Isle Royale

Population structure of Desmophyllum pertusum found along the United States eastern continental margin

Objective The connectivity and genetic structuring of populations throughout a region influence a species’ resilience and probability of recovery from anthropogenic impacts. By gaining a comprehensive understanding of population connectivity, more effective management can be prioritized. To assess the connectivity and population genetic structure of a common cold-water coral species, Desmophyllum pertusum ( Lophelia pertusa ), we performed Restriction-site Associated DNA Sequencing (RADseq) on individuals from nine sites ranging from submarine canyons off New England to the southeastern coast of the United States (SEUS) and the Gulf of Mexico (GOM). Fifty-seven individuals and 3,180 single-nucleotide polymorphisms (SNPs) were used to assess genetic differentiation. Results High connectivity exists among populations along the SEUS, yet these populations were differentiated from those to the north off New England and in Norfolk Canyon along the North Atlantic coast of the United States, as well as those in the GOM. Interestingly, Norfolk Canyon, located just north of North Carolina, and GOM populations exhibited low levels of genetic differentiation, corroborating previous microsatellite analyses and signifying gene flow between these populations. Increasing sample sizes from existing populations and including additional sampling sites over a larger geographic range would help define potential source populations and reveal fine-scale connectivity patterns among D. pertusum populations.

Atlantic coastal margin

Development of microsatellite loci for two New World vultures (Cathartidae)

Objective Use next-generation sequencing to develop microsatellite loci that will provide the variability necessary for studies of genetic diversity and population connectivity of two New World vulture species. Results We characterized 11 microsatellite loci for black vultures ( Coragyps atratus ) and 14 loci for turkey vultures ( Cathartes aura ). These microsatellite loci were grouped into 3 multiplex panels for each species. The number of alleles among black vulture samples ranged from 2 to 11, and 3 to 48 among turkey vulture samples.

BMC Research Notes

Genetic structure along an elevational gradient in Hawaiian honeycreepers reveals contrasting evolutionary responses to avian malaria

Background. The Hawaiian honeycreepers (Drepanidinae) are one of the best-known examples of an adaptive radiation, but their persistence today is threatened by the introduction of exotic pathogens and their vector, the mosquito Culex quinquefasciatus. Historically, species such as the amakihi (Hemignathus virens), the apapane (Himatione sanguinea), and the iiwi (Vestiaria coccinea) were found from the coastal lowlands to the high elevation forests, but by the late 1800's they had become extremely rare in habitats below 900 m. Recently, however, populations of amakihi and apapane have been observed in low elevation habitats. We used twelve polymorphic microsatellite loci to investigate patterns of genetic structure, and to infer responses of these species to introduced avian malaria along an elevational gradient on the eastern flanks of Mauna Loa and Kilauea volcanoes on the island of Hawaii. Results. Our results indicate that amakihi have genetically distinct, spatially structured populations that correspond with altitude. We detected very few apapane and no iiwi in low-elevation habitats, and genetic results reveal only minimal differentiation between populations at different altitudes in either of these species. Conclusion. Our results suggest that amakihi populations in low elevation habitats have not been recolonized by individuals from mid or high elevation refuges. After generations of strong selection for pathogen resistance, these populations have rebounded and amakihi have become common in regions in which they were previously rare or absent. ?? 2008 Eggert et al; licensee BioMed Central Ltd.

BMC Evolutionary Biology

New insights into the phylogenetics and population structure of the prairie falcon (Falco mexicanus)

Background Management requires a robust understanding of between- and within-species genetic variability, however such data are still lacking in many species. For example, although multiple population genetics studies of the peregrine falcon ( Falco peregrinus ) have been conducted, no similar studies have been done of the closely-related prairie falcon ( F. mexicanus ) and it is unclear how much genetic variation and population structure exists across the species’ range. Furthermore, the phylogenetic relationship of F. mexicanus relative to other falcon species is contested. We utilized a genomics approach (i.e., genome sequencing and assembly followed by single nucleotide polymorphism genotyping) to rapidly address these gaps in knowledge. Results We sequenced the genome of a single female prairie falcon and generated a 1.17 Gb (gigabases) draft genome assembly. We generated maximum likelihood phylogenetic trees using complete mitochondrial genomes as well as nuclear protein-coding genes. This process provided evidence that F. mexicanus is an outgroup to the clade that includes the peregrine falcon and members of the subgenus Hierofalco. We annotated > 16,000 genes and almost 600,000 high-quality single nucleotide polymorphisms (SNPs) in the nuclear genome, providing the raw material for a SNP assay design featuring > 140 gene-associated markers and a molecular-sexing marker. We subsequently genotyped ~ 100 individuals from California (including the San Francisco East Bay Area, Pinnacles National Park and the Mojave Desert) and Idaho (Snake River Birds of Prey National Conservation Area). We tested for population structure and found evidence that individuals sampled in California and Idaho represent a single panmictic population. Conclusions Our study illustrates how genomic resources can rapidly shed light on genetic variability in understudied species and resolve phylogenetic relationships. Furthermore, we found evidence of a single, randomly mating population of prairie falcons across our sampling locations. Prairie falcons are highly mobile and relatively rare long-distance dispersal events may promote gene flow throughout the range. As such, California’s prairie falcons might be managed as a single population, indicating that management actions undertaken to benefit the species at the local level have the potential to influence the species as a whole.

BMC Genomics

Optimization of a suite of flathead catfish (Pylodictis olivaris) microsatellite markers for understanding the population genetics of introduced populations in the northeast United States

Flathead catfish are rapidly expanding into nonnative waterways throughout the United States. Once established, flathead catfish may cause disruptions to the local ecosystem through consumption and competition with native fishes, including species of conservation concern. Flathead catfish often become a popular sport fish in their introduced range, and so management strategies must frequently balance the need to protect native and naturalized fauna while meeting the desire to maintain or enhance fisheries. However, there are currently few tools available to inform management of invasive flathead catfish ( Pylodictis olivaris ). We describe a suite of microsatellite loci that can be used to characterize population structure, predict invasion history, and assess potential mitigation strategies for flathead catfish.

Pennsylvania

Genetic diversity and connectivity of chemosynthetic cold seep mussels from the U.S. Atlantic margin

Background Deep-sea mussels in the subfamily Bathymodiolinae have unique adaptations to colonize hydrothermal-vent and cold-seep environments throughout the world ocean. These invertebrates function as important ecosystem engineers, creating heterogeneous habitat and promoting biodiversity in the deep sea. Despite their ecological significance, efforts to assess the diversity and connectivity of this group are extremely limited. Here, we present the first genomic-scale diversity assessments of the recently discovered bathymodioline cold-seep communities along the U.S. Atlantic margin, dominated by Gigantidas childressi and Bathymodiolus heckerae . Results A Restriction-site Associated DNA Sequencing (RADSeq) approach was used on 177 bathymodiolines to examine genetic diversity and population structure within and between seep sites. Assessments of genetic differentiation using single-nucleotide polymorphism (SNP) data revealed high gene flow among sites, with the shallower and more northern sites serving as source populations for deeper occurring G. childressi . No evidence was found for genetic diversification across depth in G. childressi , likely due to their high dispersal capabilities. Kinship analyses indicated a high degree of relatedness among individuals, and at least 10–20% of local recruits within a particular site. We also discovered candidate adaptive loci in G. childressi and B. heckerae that suggest differences in developmental processes and depth-related and metabolic adaptations to chemosynthetic environments. Conclusions These results highlight putative source communities for an important ecosystem engineer in the deep sea that may be considered in future conservation efforts. Our results also provide clues into species-specific adaptations that enable survival and potential speciation within chemosynthetic ecosystems.

Atlantic Ocean, Baltimore Canyon Seep, Blake Ridge

Population structure and plumage polymorphism: the intraspecific evolutionary relationships of a polymorphic raptor, Buteo jamaicensis harlani

Background Phenotypic and molecular genetic data often provide conflicting patterns of intraspecific relationships confounding phylogenetic inference, particularly among birds where a variety of environmental factors may influence plumage characters. Among diurnal raptors, the taxonomic relationship of Buteo jamaicensis harlani to other B. jamaicensis subspecies has been long debated because of the polytypic nature of the plumage characteristics used in subspecies or species designations. Results To address the evolutionary relationships within this group, we used data from 17 nuclear microsatellite loci, 430 base pairs of the mitochondrial control region, and 829 base pairs of the melanocortin 1 receptor ( Mc1r ) to investigate molecular genetic differentiation among three B. jamaicensis subspecies ( B. j. borealis , B. j. calurus , B. j. harlani ). Bayesian clustering analyses of nuclear microsatellite loci showed no significant differences between B. j. harlani and B. j. borealis . Differences observed between B. j. harlani and B. j. borealis in mitochondrial and microsatellite data were equivalent to those found between morphologically similar subspecies, B. j. borealis and B. j. calurus , and estimates of migration rates among all three subspecies were high. No consistent differences were observed in Mc1r data between B. j. harlani and other B. jamaicensis subspecies or between light and dark color morphs within B. j. calurus , suggesting that Mc1r does not play a significant role in B. jamaicensis melanism. Conclusions These data suggest recent interbreeding and gene flow between B. j. harlani and the other B. jamaicensis subspecies examined, providing no support for the historical designation of B. j. harlani as a distinct species.

BMC Evolutionary Biology

Tracing the first steps of American sturgeon pioneers in Europe

Background. A Baltic population of Atlantic sturgeon was founded ???1,200 years ago by migrants from North America, but after centuries of persistence, the population was extirpated in the 1960s, mainly as a result of over-harvest and habitat alterations. As there are four genetically distinct groups of Atlantic sturgeon inhabiting North American rivers today, we investigated the genetic provenance of the historic Baltic population by ancient DNA analyses using mitochondrial and nuclear markers. Results. The phylogeographic signal obtained from multilocus microsatellite DNA genotypes and mitochondrial DNA control region haplotypes, when compared to existing baseline datasets from extant populations, allowed for the identification of the region-of-origin of the North American Atlantic sturgeon founders. Moreover, statistical and simulation analyses of the multilocus genotypes allowed for the calculation of the effective number of individuals that originally founded the European population of Atlantic sturgeon. Our findings suggest that the Baltic population of A. oxyrinchus descended from a relatively small number of founders originating from the northern extent of the species' range in North America. Conclusion. These results demonstrate that the most northerly distributed North American A. oxyrinchus colonized the Baltic Sea ???1,200 years ago, suggesting that Canadian specimens should be the primary source of broodstock used for restoration in Baltic rivers. This study illustrates the great potential of patterns obtained from ancient DNA to identify population-of-origin to investigate historic genotype structure of extinct populations. ?? 2008 Ludwig et al; licensee BioMed Central Ltd.

BMC Evolutionary Biology

Chromosome rearrangements, recombination suppression, and limited segregation distortion in hybrids between Yellowstone cutthroat trout ( Oncorhynchus clarkii bouvieri ) and rainbow trout ( O. mykiss )

Background Introgressive hybridization is an important evolutionary process that can lead to the creation of novel genome structures and thus potentially new genetic variation for selection to act upon. On the other hand, hybridization with introduced species can threaten native species, such as cutthroat trout ( Oncorhynchus clarkii ) following the introduction of rainbow trout ( O. mykiss ). Neither the evolutionary consequences nor conservation implications of rainbow trout introgression in cutthroat trout is well understood. Therefore, we generated a genetic linkage map for rainbow-Yellowstone cutthroat trout ( O. clarkii bouvieri ) hybrids to evaluate genome processes that may help explain how introgression affects hybrid genome evolution. Results The hybrid map closely aligned with the rainbow trout map (a cutthroat trout map does not exist), sharing all but one linkage group. This linkage group (RYHyb20) represented a fusion between an acrocentric (Omy28) and a metacentric chromosome (Omy20) in rainbow trout. Additional mapping in Yellowstone cutthroat trout indicated the two rainbow trout homologues were fused in the Yellowstone genome. Variation in the number of hybrid linkage groups (28 or 29) likely depended on a Robertsonian rearrangement polymorphism within the rainbow trout stock. Comparison between the female-merged F 1 map and a female consensus rainbow trout map revealed that introgression suppressed recombination across large genomic regions in 5 hybrid linkage groups. Two of these linkage groups (RYHyb20 and RYHyb25_29) contained confirmed chromosome rearrangements between rainbow and Yellowstone cutthroat trout indicating that rearrangements may suppress recombination. The frequency of allelic and genotypic segregation distortion varied among parents and families, suggesting few incompatibilities exist between rainbow and Yellowstone cutthroat trout genomes. Conclusions Chromosome rearrangements suppressed recombination in the hybrids. This result supports several previous findings demonstrating that recombination suppression restricts gene flow between chromosomes that differ by arrangement. Conservation of synteny and map order between the hybrid and rainbow trout maps and minimal segregation distortion in the hybrids suggest rainbow and Yellowstone cutthroat trout genomes freely introgress across chromosomes with similar arrangement. Taken together, these results suggest that rearrangements impede introgression. Recombination suppression across rearrangements could enable large portions of non-recombined chromosomes to persist within admixed populations.

BMC Genomics

Effect of growth rate on transcriptomic responses to immune stimulation in wild-type, domesticated, and GH-transgenic coho salmon

Background Transcriptomic responses to immune stimulation were investigated in coho salmon (Oncorhynchus kisutch) with distinct growth phenotypes. Wild-type fish were contrasted to strains with accelerated growth arising either from selective breeding (i.e. domestication) or genetic modification. Such distinct routes to accelerated growth may have unique implications for relationships and/or trade-offs between growth and immune function. Results RNA-Seq was performed on liver and head kidney in four ‘growth response groups’ injected with polyinosinic-polycytidylic acid (Poly I:C; viral mimic), peptidoglycan (PGN; bacterial mimic) or PBS (control). These groups were: 1) ‘W’: wild-type, 2) ‘TF’: growth hormone (GH) transgenic salmon with ~ 3-fold higher growth-rate than W, 3) ‘TR’: GH transgenic fish ration restricted to possess a growth-rate equal to W, and 4) ‘D’: domesticated non-transgenic fish showing growth-rate intermediate to W and TF. D and TF showed a higher similarity in transcriptomic response compared to W and TR. Several immune genes showed constitutive expression differences among growth response groups, including perforin 1 and C-C motif chemokine 19-like. Among the affected immune pathways, most were up-regulated by Poly I:C and PGN. In response to PGN, the c-type lectin receptor signalling pathway responded uniquely in TF and TR. In response to stimulation with both immune mimics, TR responded more strongly than other groups. Further, group-specific pathway responses to PGN stimulation included NOD-like receptor signalling in W and platelet activation in TR. TF consistently showed the most attenuated immune response relative to W, and more DEGs were apparent in TR than TF and D relative to W, suggesting that a non-satiating ration coupled with elevated circulating GH levels may cause TR to possess enhanced immune capabilities. Alternatively, TF and D salmon are prevented from acquiring the same level of immune response as TR due to direction of energy to high overall somatic growth. Further study of the effects of ration restriction in growth-modified fishes is warranted. Conclusions These findings improve our understanding of the pleiotropic effects of growth modification on the immunological responses of fish, revealing unique immune pathway responses depending on the mechanism of growth acceleration and nutritional availability.

BMC Genomics