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The northern pike Esox lucius is a freshwater fish with low genetic diversity but ecological success throughout the Northern Hemisphere. Here we generate an annotated chromosome-level genome assembly of 941 Mbp in length with 25 chromosome-length scaffolds. We then genotype 47 northern pike from Alaska through New Jersey at a genome-wide scale and characterize a striking decrease in genetic diversity along the sampling range. Individuals west of the North American Continental Divide have substantially higher diversity than those to the east (e.g., Interior Alaska and St. Lawrence River have on average 181K and 64K heterozygous SNPs per individual, or a heterozygous SNP every 5.2 kbp and 14.6 kbp, respectively). Individuals clustered within each population with strong support, with numerous private alleles observed within each population. Evidence for recent population expansion was observed for a Manitoba hatchery and the St. Lawrence population (Tajima's D = -1.07 and -1.30, respectively). Several chromosomes have large regions with elevated diversity, including LG24, which holds amhby, the ancestral sex determining gene. As expected amhby was largely male-specific in Alaska and the Yukon and absent southeast to these populations, but we document some amhby(-) males in Alaska and amhby(+) males in the Columbia River, providing evidence for a patchwork of presence of this system in the western region. These results support the theory that northern pike recolonized North America from refugia in Alaska and expanded following deglaciation from west to east, with probable founder effects resulting in loss of both neutral and functional diversity (e.g., amhby).
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The Fraser River once supported massive salmon returns. However, over the last century, the largest returns have consistently been less than half of the recorded historical maximum. There is substantial interest from surrounding communities and governments to increase salmon returns for both human use and functional ecosystems. To generate resources for this endeavor, we resequenced genomes of Chinook (Oncorhynchus tshawytscha), coho (O. kisutch), and sockeye salmon (O. nerka) from the Fraser River at moderate coverage (â¼16x). A total of 954 resequenced genomes were analyzed, with 681 collected specifically for this study from tissues sampled between 1997 and 2021. An additional 273 were collected from previous studies. At the species level, Chinook salmon appeared to have 1.6-2.1x more SNPs than coho or sockeye salmon, respectively. This difference may be attributable to large historical declines of coho and sockeye salmon. At the population level, three Fraser River genetic groups were identified for each species using principal component and admixture analyses, which is consistent with previous research and supports the continued use of these groups in conservation and management efforts. Environmental factors and a migration barrier were identified as major factors influencing the boundaries of these genetic groups. Additionally, 20 potentially adaptive loci were identified among the genetic groups. This information may be valuable in new management and conservation efforts. Furthermore, the resequenced genomes are an important resource for contemporary genomics research on Fraser River salmon and have been made publicly available.
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Salmon lice, Lepeophtheirus salmonis (family Caligidae), are ectoparasites that have negatively impacted the salmon aquaculture industry and vulnerable wild salmon populations. Researchers have studied salmon lice to better understand their biology to develop effective control strategies. In this study, we updated the chromosome-level reference genome assembly of the Pacific subspecies of L. salmonis using Hi-C data. The previous version placed contigs/scaffolds using an Atlantic salmon louse genetic map. By utilizing Hi-C data from Pacific salmon lice, we were able to properly assign locations to contigs/scaffolds previously unplaced or misplaced. This resulted in a more accurate genome assembly and a more comprehensive characterization of the sex chromosome unique to females (W). We found evidence that the same ZW-ZZ mechanism is common in both Atlantic and Pacific subspecies of salmon lice using PCR assays. The W chromosome was approximately 800â kb in size, which is â¼30 times smaller than the Z chromosome (24â Mb). The W chromosome contained 61 annotated genes, including 32 protein-coding genes, 27 long noncoding RNA (lncRNA) genes, and 2 pseudogenes. Among these 61 genes, 39 genes shared homology to genes found on other chromosomes, while 20 were unique to the W chromosome. Two genes of interest on the W chromosome, prohibitin-2 and kinase suppressor of ras-2, were previously identified as potential sex-linked markers in the salmon louse. However, we prioritized the 20 unique genes on the W chromosome as sex-determining candidates. This information furthers our understanding of the biology of this ectoparasite and may help in the development of more effective management strategies.
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Copépodes , Cromossomos Sexuais , Animais , Copépodes/genética , Cromossomos Sexuais/genética , Feminino , Masculino , Genoma , Mapeamento Cromossômico , Salmão/parasitologia , Salmão/genéticaRESUMO
How various factors, including demography, recombination or genome duplication, may impact the efficacy of natural selection and the burden of deleterious mutations, is a central question in evolutionary biology and genetics. In this study, we show that key evolutionary processes, including variations in i) effective population size (Ne) ii) recombination rates and iii) chromosome inheritance, have influenced the genetic load and efficacy of selection in Coho salmon (Oncorhynchus kisutch), a widely distributed salmonid species on the west coast of North America. Using whole genome resequencing data from 14 populations at different migratory distances from their southern glacial refugium, we found evidence supporting gene surfing, wherein reduced Ne at the postglacial recolonization front, leads to a decrease in the efficacy of selection and a surf of deleterious alleles in the northernmost populations. Furthermore, our results indicate that recombination rates play a prime role in shaping the load along the genome. Additionally, we identified variation in polyploidy as a contributing factor to within-genome variation of the load. Overall, our results align remarkably well with expectations under the nearly neutral theory of molecular evolution. We discuss the fundamental and applied implications of these findings for evolutionary and conservation genomics.
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Evolução Biológica , Oncorhynchus kisutch , Animais , Alelos , Seleção Genética , Evolução Molecular , Oncorhynchus kisutch/genéticaRESUMO
Chum salmon are ecologically important to Pacific Ocean ecosystems and commercially important to fisheries. To improve the genetic resources available for this species, we sequenced and assembled the genome of a male chum salmon using Oxford Nanopore read technology and the Flye genome assembly software (contig N50: â¼2 Mbp, complete BUSCOs: â¼98.1%). We also resequenced the genomes of 59 chum salmon from hatchery sources to better characterize the genome assembly and the diversity of nucleotide variants impacting phenotype variation. With genomic sequences from a doubled haploid individual, we were able to identify regions of the genome assembly that have been collapsed due to high sequence similarity between homeologous (duplicated) chromosomes. The homeologous chromosomes are relics of an ancient salmonid-specific genome duplication. These regions were enriched with genes whose functions are related to the immune system and responses to toxins. From analyzing nucleotide variant annotations of the resequenced genomes, we were also able to identify genes that have increased levels of variants thought to moderately impact gene function. Genes related to the immune system and the detection of chemical stimuli (olfaction) had increased levels of these variants based on a gene ontology enrichment analysis. The tandem organization of many of the enriched genes raises the question of why they have this organization.
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Duplicação Gênica , Genoma , Oncorhynchus keta , Oncorhynchus keta/genética , Animais , Estudo de Associação Genômica Ampla , Masculino , Feminino , Nucleotídeos/genética , Fenótipo , Filogenia , Cromossomos , Processos de Determinação SexualRESUMO
Sablefish (Anoplopoma fimbria) are in the suborder Cottioidei, which also includes stickleback and lumpfish. This species inhabits coastal regions of the northeastern and northwestern Pacific Ocean from California to Japan. A commercial fishery for sablefish began to flourish in the 1960s, though a downward trend in stock biomass and landings has been observed since 2010. Aquaculture protocols have been developed for sablefish; eggs and sperm from wild-caught and hatchery-reared captive broodstock are used to generate offspring that reach market size in about two years. Parentage analyses show that survival in aquaculture varies among families. Growth rate and disease resistance also vary among individuals and cohorts, but the extent to which genetics and the environment contribute to this variation is unclear. The sablefish genome assembly reported here will form the foundation for SNP-based surveys designed to detect genetic markers associated with survival, growth rate, and pathogen resistance. Beyond its contribution to sablefish domestication, the sablefish genome can be a resource for the management of the wild sablefish fishery. The assembly generated in this study had a length of 653 Mbp, a scaffold N50 of 26.74 Mbp, a contig N50 of 2.57 Mbp, and contained more than 98% of the 3640 Actinopterygii core genes. We placed 620.9 Mbp (95% of the total) onto 24 chromosomes using a genetic map derived from six full-sib families and Hi-C contact data.
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Perciformes , Smegmamorpha , Humanos , Animais , Masculino , Sêmen , Perciformes/genética , Peixes/genética , Smegmamorpha/genética , CromossomosRESUMO
Coho salmon (Oncorhynchus kisutch) are a culturally and economically important species that return from multiyear ocean migrations to spawn in rivers that flow to the Northern Pacific Ocean. Southern stocks of coho salmon in Canada and the United States have significantly declined over the past quarter century, and unfortunately, conservation efforts have not reversed this trend. To assist in stock management and conservation efforts, we generated a chromosome-level genome assembly. We also resequenced the genomes of 83 coho salmon across the North American range to identify nucleotide variants and understand the demographic histories of these salmon by modeling effective population size from genome-wide data. From demographic history modeling, we observed reductions in effective population sizes between 3,750 and 8,000 years ago for several northern sampling sites, which may correspond to bottleneck events during recolonization after glacial retreat.
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Oncorhynchus kisutch , Animais , Oncorhynchus kisutch/genética , Densidade Demográfica , GenomaRESUMO
Inferring the genomic basis of local adaptation is a long-standing goal of evolutionary biology. Beyond its fundamental evolutionary implications, such knowledge can guide conservation decisions for populations of conservation and management concern. Here, we investigated the genomic basis of local adaptation in the Coho salmon (Oncorhynchus kisutch) across its entire North American range. We hypothesized that extensive spatial variation in environmental conditions and the species' homing behaviour may promote the establishment of local adaptation. We genotyped 7829 individuals representing 217 sampling locations at more than 100,000 high-quality RADseq loci to investigate how recombination might affect the detection of loci putatively under selection and took advantage of the precise description of the demographic history of the species from our previous work to draw accurate population genomic inferences about local adaptation. The results indicated that genetic differentiation scans and genetic-environment association analyses were both significantly affected by variation in recombination rate as low recombination regions displayed an increased number of outliers. By taking these confounding factors into consideration, we revealed that migration distance was the primary selective factor driving local adaptation and partial parallel divergence among distant populations. Moreover, we identified several candidate single nucleotide polymorphisms associated with long-distance migration and altitude including a gene known to be involved in adaptation to altitude in other species. The evolutionary implications of our findings are discussed along with conservation applications.
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Oncorhynchus kisutch , Humanos , Animais , Oncorhynchus kisutch/genética , Genética Populacional , Adaptação Fisiológica/genética , Deriva Genética , Genoma , Polimorfismo de Nucleotídeo Único/genéticaRESUMO
Conservation units (CUs) are important tools for supporting the implementation of standardized management practices for exploited species. Following the adoption of the Wild Salmon Policy in Canada, CUs were defined for Pacific salmon based on characteristics related to ecotype, life history and genetic variation using microsatellite markers as indirect measures of local adaptation. Genomic data sets have the potential to improve the definition of CUs by reducing variance around estimates of population genetic parameters, thereby increasing the power to detect more subtle patterns of population genetic structure and by providing an opportunity to incorporate adaptive information more directly with the identification of variants putatively under selection. We used one of the largest genomic data sets recently published for a nonmodel species, comprising 5662 individual Coho salmon (Oncorhynchus kisutch) from 149 sampling locations and a total of 24,542 high-quality SNPs obtained using genotyping-by-sequencing and mapped to the Coho salmon reference genome to (1) evaluate the current delineation of CUs for Coho in Canada and (2) compare patterns of population structure observed using neutral and outlier loci from genotype-environment association analyses to determine whether separate CUs that capture adaptive diversity are needed. Our results reflected CU boundaries on the whole, with the majority of sampling locations managed in the same CU clustering together within genetic groups. However, additional groups that are not currently represented by CUs were also uncovered. We observed considerable overlap in the genetic clusters identified using neutral or candidate loci, indicating a general congruence in patterns of genetic variation driven by local adaptation and gene flow in this species. Consequently, we suggest that the current CU boundaries for Coho salmon are largely well-suited for meeting the Canadian Wild Salmon Policy's objective of defining biologically distinct groups, but we highlight specific areas where CU boundaries may be refined.
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Salmon lice have plagued the salmon farming industry and have negatively impacted salmon populations in the wild. In response, researchers have generated high density genetic maps, genome assemblies, transcriptomes, and whole-genome resequencing data to better understand this parasite. In this study, we used long-read sequencing technology to update the previous genome assemblies of Atlantic Ocean salmon lice with a more contiguous assembly and a more comprehensive gene catalog of Pacific Ocean salmon lice. We were also able to further characterize genomic features previously identified from other studies by using published resequenced genomes of 25 Atlantic and 15 Pacific salmon lice. One example was further characterizing the ZW sex chromosomes. For both the Atlantic and Pacific Ocean salmon lice subspecies, we found that the female W-chromosome is only a small fraction of the Z-chromosome and that the vast majority of the W and Z-chromosome do not contain conserved regions (i.e. pseudoautosomal regions). However, conserved orthologous protein sequences can still be identified between the W- and Z-chromosomes.
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Copépodes , Doenças dos Peixes , Salmo salar , Animais , Copépodes/genética , Feminino , Doenças dos Peixes/genética , Doenças dos Peixes/parasitologia , Oceano Pacífico , Salmo salar/genética , Salmão/genética , Análise de Sequência de DNA , TranscriptomaRESUMO
AbstractThe potentially significant genetic consequences associated with the loss of migratory capacity of diadromous fishes that have become landlocked in freshwater are poorly understood. Consistent selective pressures associated with freshwater residency may drive repeated differentiation both between allopatric landlocked and anadromous populations and within landlocked populations (resulting in sympatric morphs). Alternatively, the strong genetic drift anticipated in isolated landlocked populations could hinder consistent adaptation, limiting genetic parallelism. Understanding the degree of genetic parallelism underlying differentiation has implications for both the predictability of evolution and management practices. We employed an 87k single-nucleotide polymorphism (SNP) array to examine the genetic characteristics of landlocked and anadromous Arctic char (Salvelinus alpinus) populations from five drainages within Labrador, Canada. One gene was detected as an outlier between sympatric, size-differentiated morphs in each of two landlocked lakes. While no single locus differentiated all replicate pairs of landlocked and anadromous populations, several SNPs, genes, and paralogs were consistently detected as outliers in at least 70% of these pairwise comparisons. A significant C-score suggested that the amount of shared outlier SNPs across all paired landlocked and anadromous populations was greater than expected by chance. Our results indicate that despite their isolation, selection due to the loss of diadromy may drive consistent genetic responses in landlocked populations.
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Lagos , Truta , Animais , Regiões Árticas , Genoma , Genômica , Truta/genéticaRESUMO
Pink salmon (Oncorhynchus gorbuscha) adults are the smallest of the five Pacific salmon native to the western Pacific Ocean. Pink salmon are also the most abundant of these species and account for a large proportion of the commercial value of the salmon fishery worldwide. A two-year life history of pink salmon generates temporally isolated populations that spawn either in even-years or odd-years. To uncover the influence of this genetic isolation, reference genome assemblies were generated for each year-class and whole genome re-sequencing data was collected from salmon of both year-classes. The salmon were sampled from six Canadian rivers and one Japanese river. At multiple centromeres we identified peaks of Fst between year-classes that were millions of base-pairs long. The largest Fst peak was also associated with a million base-pair chromosomal polymorphism found in the odd-year genome near a centromere. These Fst peaks may be the result of a centromere drive or a combination of reduced recombination and genetic drift, and they could influence speciation. Other regions of the genome influenced by odd-year and even-year temporal isolation and tentatively under selection were mostly associated with genes related to immune function, organ development/maintenance, and behaviour.
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Proteínas de Peixes/genética , Especiação Genética , Genoma , Estágios do Ciclo de Vida/genética , Reprodução/genética , Salmão/genética , Animais , Canadá , Feminino , Proteínas de Peixes/classificação , Proteínas de Peixes/metabolismo , Expressão Gênica , Genética Populacional , Genômica/métodos , Japão , Masculino , Oceano Pacífico , Polimorfismo Genético , Isolamento Reprodutivo , Rios , Salmão/classificação , Salmão/crescimento & desenvolvimento , Salmão/metabolismo , Sequenciamento Completo do GenomaRESUMO
[This corrects the article DOI: 10.1371/journal.pone.0240935.].
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Copepods encompass numerous ecological roles including parasites, detrivores and phytoplankton grazers. Nonetheless, copepod genome assemblies remain scarce. Lepeophtheirus salmonis is an economically and ecologically important ectoparasitic copepod found on salmonid fish. We present the 695.4 Mbp L. salmonis genome assembly containing ≈60% repetitive regions and 13,081 annotated protein-coding genes. The genome comprises 14 autosomes and a ZZ-ZW sex chromosome system. Assembly assessment identified 92.4% of the expected arthropod genes. Transcriptomics supported annotation and indicated a marked shift in gene expression after host attachment, including apparent downregulation of genes related to circadian rhythm coinciding with abandoning diurnal migration. The genome shows evolutionary signatures including loss of genes needed for peroxisome biogenesis, presence of numerous FNII domains, and an incomplete heme homeostasis pathway suggesting heme proteins to be obtained from the host. Despite repeated development of resistance against chemical treatments L. salmonis exhibits low numbers of many genes involved in detoxification.
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Copépodes , Doenças dos Peixes , Parasitos , Aclimatação , Animais , Copépodes/genética , Copépodes/parasitologia , Doenças dos Peixes/genética , Parasitos/genética , TranscriptomaRESUMO
The post-glacial colonization of Gander Lake in Newfoundland, Canada, by Arctic Charr (Salvelinus alpinus) provides the opportunity to study the genomic basis of adaptation to extreme deep-water environments. Colonization of deep-water (>50 m) habitats often requires extensive adaptation to cope with novel environmental challenges from high hydrostatic pressure, low temperature, and low light, but the genomic mechanisms underlying evolution in these environments are rarely known. Here, we compare genomic divergence between a deep-water morph adapted to depths of up to 288 m and a larger, piscivorous pelagic morph occupying shallower depths. Using both a SNP array and resequencing of whole nuclear and mitochondrial genomes, we find clear genetic divergence (FST = 0.11-0.15) between deep and shallow water morphs, despite an absence of morph divergence across the mitochondrial genome. Outlier analyses identified many diverged genomic regions containing genes enriched for processes such as gene expression and DNA repair, cardiac function, and membrane transport. Detection of putative copy number variants (CNVs) uncovered 385 genes with CNVs distinct to piscivorous morphs, and 275 genes with CNVs distinct to deep-water morphs, enriched for processes associated with synapse assembly. Demographic analyses identified evidence for recent and local morph divergence, and ongoing reductions in diversity consistent with postglacial colonization. Together, these results show that Arctic Charr morph divergence has occurred through genome-wide differentiation and elevated divergence of genes underlying multiple cellular and physiological processes, providing insight into the genomic basis of adaptation in a deep-water habitat following postglacial recolonization.
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Truta , Água , Adaptação Fisiológica/genética , Animais , Genoma , Genômica , Truta/genéticaRESUMO
BACKGROUND: Whole genome duplication (WGD) events have played a major role in eukaryotic genome evolution, but the consequence of these extreme events in adaptive genome evolution is still not well understood. To address this knowledge gap, we used a comparative phylogenetic model and transcriptomic data from seven species to infer selection on gene expression in duplicated genes (ohnologs) following the salmonid WGD 80-100 million years ago. RESULTS: We find rare cases of tissue-specific expression evolution but pervasive expression evolution affecting many tissues, reflecting strong selection on maintenance of genome stability following genome doubling. Ohnolog expression levels have evolved mostly asymmetrically, by diverting one ohnolog copy down a path towards lower expression and possible pseudogenization. Loss of expression in one ohnolog is significantly associated with transposable element insertions in promoters and likely driven by selection on gene dosage including selection on stoichiometric balance. We also find symmetric expression shifts, and these are associated with genes under strong evolutionary constraints such as ribosome subunit genes. This possibly reflects selection operating to achieve a gene dose reduction while avoiding accumulation of "toxic mutations". Mechanistically, ohnolog regulatory divergence is dictated by the number of bound transcription factors in promoters, with transposable elements being one likely source of novel binding sites driving tissue-specific gains in expression. CONCLUSIONS: Our results imply pervasive adaptive expression evolution following WGD to overcome the immediate challenges posed by genome doubling and to exploit the long-term genetic opportunities for novel phenotype evolution.
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Evolução Molecular , Dosagem de Genes , Duplicação Gênica , Genoma , Genômica/métodos , Seleção Genética , Regulação da Expressão Gênica , Genes Essenciais , Fígado/metabolismo , Especificidade de Órgãos/genética , FilogeniaRESUMO
Genotype-by-environment (GxE) interactions are non-parallel reaction norms among individuals with different genotypes in response to different environmental conditions. GxE interactions are an extension of phenotypic plasticity and consequently studying such interactions improves our ability to predict effects of different environments on phenotype as well as the fitness of genetically distinct organisms and their capacity to interact with ecosystems. Growth hormone transgenic coho salmon grow much faster than non-transgenics when raised in tank environments, but show little difference in growth when reared in nature-like streams. We used this model system to evaluate potential mechanisms underlying this growth rate GxE interaction, performing RNA-seq to measure gene transcription and whole-genome bisulfite sequencing to measure gene methylation in liver tissue. Gene ontology (GO) term analysis revealed stress as an important biological process potentially influencing growth rate GxE interactions. While few genes with transcription differences also had methylation differences, in promoter or gene regions, many genes were differentially methylated between tank and stream environments. A GO term analysis of differentially methylated genes between tank and stream environments revealed increased methylation in the stream environment of more than 95% of the differentially methylated genes, many with biological processes unrelated to liver function. The lower nutritional condition of the stream environment may cause increased negative regulation of genes less vital for liver tissue function than when fish are reared in tanks with unlimited food availability. These data show a large effect of rearing environment both on gene expression and methylation, but it is less clear that the detected epigenetic marks are responsible for the observed altered growth and physiological responses.
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Ecossistema , Oncorhynchus kisutch , Animais , Epigênese Genética , Interação Gene-Ambiente , Genótipo , Oncorhynchus kisutch/genética , Fenótipo , TranscriptomaRESUMO
[This corrects the article DOI: 10.1371/journal.pgen.1008348.].
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Growth hormone (GH) transgenic fish often exhibit remarkable transformations in growth rate and other phenotypes relative to wild-type. The 5750A transgenic coho salmon strain exhibits strong sexually dimorphic growth, with females possessing growth stimulation at a level typical of that seen for both sexes in other strains harbouring the same gene construct (e.g. M77), while males display a modest level of growth stimulation. GH mRNA levels were significantly higher in females than in males of the 5750A strain but equivalent in the M77 strain, indicating sex and transgene insertion locus altered transgene expression. We found that acute estradiol treatments did not influence GH expression in either strain (5750A and M77) or the transgene promoter (metallothionein-B), suggesting that estradiol level was not a significant factor influencing transgene activity. The feminization of XX and XY fish of the 5750A and M77 strains generated all-female groups and resulted in equalized growth of the two genetic sexes, suggesting that the presence of the Y chromosome was not directly capable of influencing the GH transgene-mediated growth in a physiological female conditions. These data suggest that the difference in growth rate seen between the sexes in the 5750A strain arises from non-estradiol-mediated sex influences on gene regulation at the transgene locus. This study shows how genetic factors and transgene insertion sites can influence transgene expression with significant consequent effects on phenotype.