Seasonal Variation in the Skin Transcriptome of Common Bottlenose Dolphins (Tursiops truncatus) from the Northern Gulf of Mexico

Dolah, Frances M. Van; Neely, Marion G.; McGeorge, Lauren E.; Balmer, Brian C.; Ylitalo, Gina M.; Zolman, Eric S.; Speakman, Todd; Sinclair, Carrie; Kellar, Nicholas M.; Rosel, Patricia E.; Mullin, Keith D.; Schwacke, Lori H.

doi:10.1371/journal.pone.0130934

Cited by 32 publications

(25 citation statements)

References 49 publications

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“…For example, managed spinner dolphins ( Stenella longirostris ) exhibit seasonal variations in testosterone concentration ( 48 ). Seasonal changes in blood chemistry values and the skin transcriptome have also been documented in bottlenose dolphins ( 49 , 50 ). Although not overwhelmingly correlated, sex hormones have been weakly correlated with adiponectin levels in humans ( 51 , 52 ).…”

Section: Discussionmentioning

confidence: 94%

Feeding a Modified Fish Diet to Bottlenose Dolphins Leads to an Increase in Serum Adiponectin and Sphingolipids

et al. 2016

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Feeding a modified fish diet has been suggested to improve insulin sensitivity in bottlenose dolphins; however, insulin sensitivity was not directly measured. Since demonstrating an improvement in insulin sensitivity is technically difficult in dolphins, we postulated that directional changes in the hormone axis: fibroblast growth factor 21 (FGF21)/Adiponectin/Ceramide (Cer), could provide further support to this hypothesis. We measured 2-h post-prandial serum FGF21, total adiponectin, percent unmodified adiponectin, ceramide, and sphingosine levels from dolphins fed a diet rich in heptadecanoic acid (C17:0) over 24 weeks. Serum FGF21 was quantified by ELISA with an observed range of 129–1599 pg/ml, but did not significantly change over the 24-week study period. Total adiponectin levels (mean ± SD) significantly increased from 776 ± 400 pmol/ml at week 0 to 1196 ± 467 pmol/ml at week 24. The percent unmodified adiponectin levels (mean ± SD) decreased from 23.8 ± 6.0% at week 0 to 15.2 ± 5.2% at week 24. Interestingly, although FGF21 levels did not change, there was a good correlation between FGF21 and total adiponectin (ρ = 0.788, P < 0.001). We quantified the abundances of serum ceramides and sphingosines (SPH) because adiponectin has a defined role in sphingolipid metabolism through adiponectin receptor-mediated activation of ceramidases. The most abundant ceramide in dolphin sera was Cer 24:1 comprising 49% of the ceramides measured. Significant reductions were observed in the unsaturated Cer 18:1, Cer 20:1, and Cer 24:1, whereas significant increases were observed in saturated Cer 22:0, Cer 24:0, and Cer 26:0. However, total serum ceramides did not change. Significant elevations were detected for total sphingosine, dihydrosphingosine, sphingosine-1-phosphate, and dihydrosphingosine-1-phosphate. Proteomic analysis of the serum proteins revealed few changes in serum proteins over the study period. In conclusion, shifting the dolphin diet to fishes rich in odd chain saturated fatty acids, such as C17:0, resulted in increased serum levels of the insulin sensitizing hormone adiponectin and serum SPH consistent with an insulin-sensitizing phenotype. It is still unclear whether FGF21 plays a role in the regulation of adiponectin in dolphins, similar to that shown in laboratory animal models.

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Section: Discussionmentioning

confidence: 94%

Feeding a Modified Fish Diet to Bottlenose Dolphins Leads to an Increase in Serum Adiponectin and Sphingolipids

et al. 2016

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“…These field techniques included: photo-identification (photo-ID) capture-recapture surveys to estimate abundance and survival; satellite-linked telemetry to study ranging and movements patterns; capture-release health assessments; remote biopsy sampling to study stock structure, contaminant loads, stable isotopes and reproductive hormones; and targeted surveys to relocate specific individuals for monitoring of reproductive outcomes (e.g. [ 9 – 12 ]).…”

Section: Introductionmentioning

confidence: 99%

Density, abundance, survival, and ranging patterns of common bottlenose dolphins (Tursiops truncatus) in Mississippi Sound following the Deepwater Horizon oil spill

et al. 2017

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After the Deepwater Horizon (DWH) oil spill began in April 2010, studies were initiated on northern Gulf of Mexico common bottlenose dolphins (Tursiops truncatus) in Mississippi Sound (MSS) to determine density, abundance, and survival, during and after the oil spill, and to compare these results to previous research in this region. Seasonal boat-based photo-identification surveys (2010–2012) were conducted in a section of MSS to estimate dolphin density and survival, and satellite-linked telemetry (2013) was used to determine ranging patterns. Telemetry suggested two different ranging patterns in MSS: (1) inshore waters with seasonal movements into mid-MSS, and (2) around the barrier islands exclusively. Based upon these data, dolphin density was estimated in two strata (Inshore and Island) using a spatially-explicit robust-design capture-recapture model. Inshore and Island density varied between 0.77–1.61 dolphins km−2 ( = 1.42, 95% CI: 1.28–1.53) and 3.32–5.74 dolphins km−2 ( = 4.43, 95% CI: 2.70–5.63), respectively. The estimated annual survival rate for dolphins with distinctive fins was very low in the year following the spill, 0.73 (95% CI: 0.67–0.78), and consistent with the occurrence of a large scale cetacean unusual mortality event that was in part attributed to the DWH oil spill. Fluctuations in density were not as large or seasonally consistent as previously reported. Total abundance for MSS extrapolated from density results ranged from 4,610 in July 2011 to 3,046 in January 2012 ( = 3,469, 95% CI: 3,113–3,725).

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“…As significant seasonal changes in transcript expression have been observed in human blood [ 11 ] and dolphin skin [ 43 ], we queried this data set for transcripts differentially expressed between summer and winter. Based on local temperatures, samples from July, August, and September were collectively defined as summer ( n = 8) while samples from December and February were defined as winter ( n = 8).…”

Section: Resultsmentioning

confidence: 99%

RNA-Seq analysis of seasonal and individual variation in blood transcriptomes of healthy managed bottlenose dolphins

et al. 2016

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BackgroundThe blood transcriptome can reflect both systemic exposures and pathological changes in other organs of the body because immune cells recirculate through the blood, lymphoid tissues, and affected sites. In human and veterinary medicine, blood transcriptome analysis has been used successfully to identify markers of disease or pathological conditions, but can be confounded by large seasonal changes in expression. In comparison, the use of transcriptomic based analyses in wildlife has been limited. Here we report a longitudinal study of four managed bottlenose dolphins located in Waikoloa, Hawaii, serially sampled (approximately monthly) over the course of 1 year to establish baseline information on the content and variation of the dolphin blood transcriptome.ResultsIllumina based RNA-seq analyses were carried out using both the Ensembl dolphin genome and a de novo blood transcriptome as guides. Overall, the blood transcriptome encompassed a wide array of cellular functions and processes and was relatively stable within and between animals over the course of 1 year. Principal components analysis revealed moderate clustering by sex associated with the variation among global gene expression profiles (PC1, 22 % of variance). Limited seasonal change was observed, with < 2.5 % of genes differentially expressed between winter and summer months (FDR < 0.05). Among the differentially expressed genes, cosinor analysis identified seasonal rhythmicity for the observed changes in blood gene expression, consistent with studies in humans. While the proportion of seasonally variant genes in these dolphins is much smaller than that reported in humans, the majority of those identified in dolphins were also shown to vary with season in humans. Gene co-expression network analysis identified several gene modules with significant correlation to age, sex, or hematological parameters.ConclusionsThis longitudinal analysis of healthy managed dolphins establishes a preliminary baseline for blood transcriptome analysis in this species. Correlations with hematological parameters, distinct from muted seasonal effects, suggest that the otherwise relatively stable blood transcriptome may be a useful indicator of health and exposure. A robust database of gene expression in free-ranging and managed dolphins across seasons with known adverse health conditions or contaminant exposures will be needed to establish predictive gene expression profiles suitable for biomonitoring.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-3020-8) contains supplementary material, which is available to authorized users.

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Seasonal Variation in the Skin Transcriptome of Common Bottlenose Dolphins (Tursiops truncatus) from the Northern Gulf of Mexico

Cited by 32 publications

References 49 publications

Feeding a Modified Fish Diet to Bottlenose Dolphins Leads to an Increase in Serum Adiponectin and Sphingolipids

Feeding a Modified Fish Diet to Bottlenose Dolphins Leads to an Increase in Serum Adiponectin and Sphingolipids

Density, abundance, survival, and ranging patterns of common bottlenose dolphins (Tursiops truncatus) in Mississippi Sound following the Deepwater Horizon oil spill

RNA-Seq analysis of seasonal and individual variation in blood transcriptomes of healthy managed bottlenose dolphins

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