Divergent transcriptomic signatures in response to salinity exposure in two populations of an estuarine fish

Ken M. Jeffries, Richard E Connon, Christine E. Verhille, Theresa F. Dabruzzi, Monica T. Britton, Blythe P. Durbin-Johnson, Nann A. Fangue

Research output: Contribution to journalArticle

1 Citation (Scopus)

Abstract

In estuary and coastal systems, human demand for freshwater, climate change-driven precipitation variability, and extreme weather impact salinity levels, reducing connectivity between mesohaline coastal fish populations and potentially contributing to genomic divergence. We examined gill transcriptome responses to salinity in wild-caught juveniles from two populations of Sacramento splittail (Pogonichthys macrolepidotus), a species of conservation concern that is endemic to the San Francisco Estuary, USA, and the lower reaches of its tributaries. Recent extreme droughts have led to salinities above the tolerance limits for this species, creating a migration barrier between these populations, which potentially contributed to population divergence. We identified transcripts involved in a conserved response to salinity; however, the more salinity-tolerant San Pablo population had greater transcriptome plasticity (3.6-fold more transcripts responded than the Central Valley population) and a response consistent with gill remodeling after 168 hr of exposure to elevated salinity. The reorganization of the gill in response to changing osmotic gradients is a process critical for acclimation and would facilitate enhanced salinity tolerance. We detected an upregulation of receptors that control the Wnt (wingless-type) cell signaling pathway that may be required for an adaptive response to increases in salinity, patterns not observed in the relatively salinity-sensitive Central Valley population. We detected 62 single nucleotide polymorphisms (SNPs) in coding regions of 26 transcripts that differed between the populations. Eight transcripts that contained SNPs were associated with immune responses, highlighting the importance of diversity in immune gene sequences as a defining characteristic of genomic divergence between these populations. Our data demonstrate that these populations have divergent transcriptomic responses to salinity, which is consistent with observed physiological differences in salinity tolerance.

Original languageEnglish (US)
Pages (from-to)1212-1226
Number of pages15
JournalEvolutionary Applications
Volume12
Issue number6
DOIs
StatePublished - Jun 1 2019

Fingerprint

estuarine fish
Salinity
transcriptomics
Fishes
salinity
fish
Population
salinity tolerance
divergence
Estuaries
gills
genomics
polymorphism
Transcriptome
transcriptome
single nucleotide polymorphism
Single Nucleotide Polymorphism
estuary
exposure
valley

Keywords

  • coastal fishes
  • extreme drought
  • genomic divergence
  • Sacramento splittail
  • single nucleotide polymorphism
  • transcriptome plasticity

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Genetics
  • Agricultural and Biological Sciences(all)

Cite this

Jeffries, K. M., Connon, R. E., Verhille, C. E., Dabruzzi, T. F., Britton, M. T., Durbin-Johnson, B. P., & Fangue, N. A. (2019). Divergent transcriptomic signatures in response to salinity exposure in two populations of an estuarine fish. Evolutionary Applications, 12(6), 1212-1226. https://doi.org/10.1111/eva.12799

Divergent transcriptomic signatures in response to salinity exposure in two populations of an estuarine fish. / Jeffries, Ken M.; Connon, Richard E; Verhille, Christine E.; Dabruzzi, Theresa F.; Britton, Monica T.; Durbin-Johnson, Blythe P.; Fangue, Nann A.

In: Evolutionary Applications, Vol. 12, No. 6, 01.06.2019, p. 1212-1226.

Research output: Contribution to journalArticle

Jeffries, KM, Connon, RE, Verhille, CE, Dabruzzi, TF, Britton, MT, Durbin-Johnson, BP & Fangue, NA 2019, 'Divergent transcriptomic signatures in response to salinity exposure in two populations of an estuarine fish', Evolutionary Applications, vol. 12, no. 6, pp. 1212-1226. https://doi.org/10.1111/eva.12799
Jeffries, Ken M. ; Connon, Richard E ; Verhille, Christine E. ; Dabruzzi, Theresa F. ; Britton, Monica T. ; Durbin-Johnson, Blythe P. ; Fangue, Nann A. / Divergent transcriptomic signatures in response to salinity exposure in two populations of an estuarine fish. In: Evolutionary Applications. 2019 ; Vol. 12, No. 6. pp. 1212-1226.
@article{f1fa5a16c26a4233a00637b0208652cc,
title = "Divergent transcriptomic signatures in response to salinity exposure in two populations of an estuarine fish",
abstract = "In estuary and coastal systems, human demand for freshwater, climate change-driven precipitation variability, and extreme weather impact salinity levels, reducing connectivity between mesohaline coastal fish populations and potentially contributing to genomic divergence. We examined gill transcriptome responses to salinity in wild-caught juveniles from two populations of Sacramento splittail (Pogonichthys macrolepidotus), a species of conservation concern that is endemic to the San Francisco Estuary, USA, and the lower reaches of its tributaries. Recent extreme droughts have led to salinities above the tolerance limits for this species, creating a migration barrier between these populations, which potentially contributed to population divergence. We identified transcripts involved in a conserved response to salinity; however, the more salinity-tolerant San Pablo population had greater transcriptome plasticity (3.6-fold more transcripts responded than the Central Valley population) and a response consistent with gill remodeling after 168 hr of exposure to elevated salinity. The reorganization of the gill in response to changing osmotic gradients is a process critical for acclimation and would facilitate enhanced salinity tolerance. We detected an upregulation of receptors that control the Wnt (wingless-type) cell signaling pathway that may be required for an adaptive response to increases in salinity, patterns not observed in the relatively salinity-sensitive Central Valley population. We detected 62 single nucleotide polymorphisms (SNPs) in coding regions of 26 transcripts that differed between the populations. Eight transcripts that contained SNPs were associated with immune responses, highlighting the importance of diversity in immune gene sequences as a defining characteristic of genomic divergence between these populations. Our data demonstrate that these populations have divergent transcriptomic responses to salinity, which is consistent with observed physiological differences in salinity tolerance.",
keywords = "coastal fishes, extreme drought, genomic divergence, Sacramento splittail, single nucleotide polymorphism, transcriptome plasticity",
author = "Jeffries, {Ken M.} and Connon, {Richard E} and Verhille, {Christine E.} and Dabruzzi, {Theresa F.} and Britton, {Monica T.} and Durbin-Johnson, {Blythe P.} and Fangue, {Nann A.}",
year = "2019",
month = "6",
day = "1",
doi = "10.1111/eva.12799",
language = "English (US)",
volume = "12",
pages = "1212--1226",
journal = "Evolutionary Applications",
issn = "1752-4563",
publisher = "Wiley-Blackwell",
number = "6",

}

TY - JOUR

T1 - Divergent transcriptomic signatures in response to salinity exposure in two populations of an estuarine fish

AU - Jeffries, Ken M.

AU - Connon, Richard E

AU - Verhille, Christine E.

AU - Dabruzzi, Theresa F.

AU - Britton, Monica T.

AU - Durbin-Johnson, Blythe P.

AU - Fangue, Nann A.

PY - 2019/6/1

Y1 - 2019/6/1

N2 - In estuary and coastal systems, human demand for freshwater, climate change-driven precipitation variability, and extreme weather impact salinity levels, reducing connectivity between mesohaline coastal fish populations and potentially contributing to genomic divergence. We examined gill transcriptome responses to salinity in wild-caught juveniles from two populations of Sacramento splittail (Pogonichthys macrolepidotus), a species of conservation concern that is endemic to the San Francisco Estuary, USA, and the lower reaches of its tributaries. Recent extreme droughts have led to salinities above the tolerance limits for this species, creating a migration barrier between these populations, which potentially contributed to population divergence. We identified transcripts involved in a conserved response to salinity; however, the more salinity-tolerant San Pablo population had greater transcriptome plasticity (3.6-fold more transcripts responded than the Central Valley population) and a response consistent with gill remodeling after 168 hr of exposure to elevated salinity. The reorganization of the gill in response to changing osmotic gradients is a process critical for acclimation and would facilitate enhanced salinity tolerance. We detected an upregulation of receptors that control the Wnt (wingless-type) cell signaling pathway that may be required for an adaptive response to increases in salinity, patterns not observed in the relatively salinity-sensitive Central Valley population. We detected 62 single nucleotide polymorphisms (SNPs) in coding regions of 26 transcripts that differed between the populations. Eight transcripts that contained SNPs were associated with immune responses, highlighting the importance of diversity in immune gene sequences as a defining characteristic of genomic divergence between these populations. Our data demonstrate that these populations have divergent transcriptomic responses to salinity, which is consistent with observed physiological differences in salinity tolerance.

AB - In estuary and coastal systems, human demand for freshwater, climate change-driven precipitation variability, and extreme weather impact salinity levels, reducing connectivity between mesohaline coastal fish populations and potentially contributing to genomic divergence. We examined gill transcriptome responses to salinity in wild-caught juveniles from two populations of Sacramento splittail (Pogonichthys macrolepidotus), a species of conservation concern that is endemic to the San Francisco Estuary, USA, and the lower reaches of its tributaries. Recent extreme droughts have led to salinities above the tolerance limits for this species, creating a migration barrier between these populations, which potentially contributed to population divergence. We identified transcripts involved in a conserved response to salinity; however, the more salinity-tolerant San Pablo population had greater transcriptome plasticity (3.6-fold more transcripts responded than the Central Valley population) and a response consistent with gill remodeling after 168 hr of exposure to elevated salinity. The reorganization of the gill in response to changing osmotic gradients is a process critical for acclimation and would facilitate enhanced salinity tolerance. We detected an upregulation of receptors that control the Wnt (wingless-type) cell signaling pathway that may be required for an adaptive response to increases in salinity, patterns not observed in the relatively salinity-sensitive Central Valley population. We detected 62 single nucleotide polymorphisms (SNPs) in coding regions of 26 transcripts that differed between the populations. Eight transcripts that contained SNPs were associated with immune responses, highlighting the importance of diversity in immune gene sequences as a defining characteristic of genomic divergence between these populations. Our data demonstrate that these populations have divergent transcriptomic responses to salinity, which is consistent with observed physiological differences in salinity tolerance.

KW - coastal fishes

KW - extreme drought

KW - genomic divergence

KW - Sacramento splittail

KW - single nucleotide polymorphism

KW - transcriptome plasticity

UR - http://www.scopus.com/inward/record.url?scp=85068065786&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85068065786&partnerID=8YFLogxK

U2 - 10.1111/eva.12799

DO - 10.1111/eva.12799

M3 - Article

AN - SCOPUS:85068065786

VL - 12

SP - 1212

EP - 1226

JO - Evolutionary Applications

JF - Evolutionary Applications

SN - 1752-4563

IS - 6

ER -