Reduced up-regulation of gene expression in response to elevated temperatures in the mid-Atlantic population of Calanus finmarchicus

Smolina, Irina; Harmer, Rachel A.; Lindeque, Penelope K.; Hoarau, Galice

doi:10.1016/j.jembe.2016.09.003

Cited by 5 publications

(3 citation statements)

References 81 publications

(103 reference statements)

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“…They play an important role in transferring energy from primary producers to secondary consumers and are therefore tightly linked to global biogeochemical systems (Menden‐Deuer & Kiørboe, ), marine trophic webs (Turner, ), and commercial fisheries (Castonguay, Plourde, Robert, Runge, & Fortier, ; Dam & Baumann, ; Friedland et al, ). Studies of thermal adaptation in copepods have a long history (Bradley, ; Lonsdale & Levinton, ), but local adaptation has largely been ignored, especially in pelagic species (but see, Smolina, Harmer, Lindeque, & Hoarau, ). The calanoid copepod Acartia tonsa often dominates coastal and estuarine environments.…”

Section: Introductionmentioning

confidence: 99%

Integrating patterns of thermal tolerance and phenotypic plasticity with population genetics to improve understanding of vulnerability to warming in a widespread copepod

Sasaki

Dam

2019

Global Change Biology

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Differences in population vulnerability to warming are defined by spatial patterns in thermal adaptation. These patterns may be driven by natural selection over spatial environmental gradients, but can also be shaped by gene flow, especially in marine taxa with high dispersal potential. Understanding and predicting organismal responses to warming requires disentangling the opposing effects of selection and gene flow. We begin by documenting genetic divergence of thermal tolerance and developmental phenotypic plasticity. Ten populations of the widespread copepod Acartia tonsa were collected from sites across a large thermal gradient, ranging from the Florida Keys to Northern New Brunswick, Canada (spanning over 20° latitude). Thermal performance curves (TPCs) from common garden experiments revealed local adaptation at the sampling range extremes, with thermal tolerance increasing at low latitudes and decreasing at high latitudes. The opposite pattern was observed in phenotypic plasticity, which was strongest at high latitudes. No relationship was observed between phenotypic plasticity and environmental variables. Instead, the results are consistent with the hypothesis of a trade-off between thermal tolerance and the strength of phenotypic plasticity. Over a large portion of the sampled range, however, we observed a remarkable lack of differentiation of TPCs. To examine whether this lack of divergence is the result of selection for a generalist performance curve or constraint by gene flow, we analyzed cytochrome oxidase I mtDNA sequences, which revealed four distinct genetic clades, abundant genetic diversity, and widely distributed haplotypes. Strong divergence in thermal performance within genetic clades, however, suggests that the pace of thermal adaptation can be relatively rapid. The combined insight from the laboratory physiological experiments and genetic data indicate that gene flow constrains differentiation of TPCs. This balance between gene flow and selection has implications for patterns of vulnerability to warming. Taking both genetic differentiation and phenotypic plasticity into account, our results suggest that local adaptation does not increase vulnerability to warming, and that low-latitude populations in general may be more vulnerable to predicted temperature change over the next century.

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Section: Introductionmentioning

confidence: 99%

Integrating patterns of thermal tolerance and phenotypic plasticity with population genetics to improve understanding of vulnerability to warming in a widespread copepod

Sasaki

Dam

2019

Global Change Biology

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“…Heat shock proteins (hsps), especially heat shock protein 70 kDa (hsp70), have been frequently used as a transcriptional indicator of stress in copepods (Voznesensky et al, 2004;Tartarotti and Torres, 2009;Lauritano et al, 2011Lauritano et al, , 2016Nilsson et al, 2013;Chan et al, 2014;Petkeviciute et al, 2015;Aguilera et al, 2016;Smolina et al, 2016;Rahlff et al, 2017). We found significant, but small, down-regulation of hsp70 in response to salinity shock 24 h after exposure (Supplementary Material S1; https://figshare.…”

Section: Discussionmentioning

confidence: 93%

Environmental Stress Responses and Experimental Handling Artifacts of a Model Organism, the Copepod Acartia tonsa (Dana)

et al. 2018

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Handling animals during experiments potentially affects the differential expression of genes chosen as biomarkers of sub-lethal stress. RNA sequencing was used to examine whole-transcriptome responses caused by laboratory handling of the calanoid copepod, Acartia tonsa. Salinity shock (S = 35 to S = 5) was used as positive stress control; individuals not exposed to handling or other stressors served as negative stress control. All copepods were grown from eggs to adults without being handled or exposed to any stressors prior the experiment. Survival of nauplii and adults was estimated for up to 10 min of exposure to handling stress and salinity shock. Only adults exhibited decreased survival (44 ± 7% with 10 min of exposure) in response to handling stress and were selected for definitive experiments for RNA sequencing. After 10 min of experimental exposures to handling stress or salinity shock, adults were incubated for 15 min or 24 h at normal culture conditions. A small number of significantly differentially expressed genes (DEGs) were observed 15 min after exposure to handling stress (2 DEGs) or salinity shock (7 DEGs). However, 24 h after exposure, handling stress resulted in 276 DEGs and salinity shock resulted in 573 DEGs, of which 174 DEGs were overlapping between the treatments. Among the DEGs observed 24 h after exposure to handling stress or salinity shock, some commonly-used stress biomarkers appeared at low levels. This suggests that a stress-response was induced at the transcriptional level for these genes between 15 min and 24 h following exposure. Since handling stress clearly affects transcriptional patterns, it is important to consider handling when designing experiments, by either including additional controls or avoiding focus on impacted genes. Not considering handling in gene expression studies can lead to inaccurate conclusions. The present study provides a baseline for studying handling stress in future studies using this model organism and others.

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“…There are a number of such studies of marine zooplankton, including target-gene and whole-transcriptome analyses of differential gene expression patterns associated with stress responses and environmental variability (Lauritano et al 2012;Schoville et al 2012;De Pittà et al 2013;Smolina et al 2015Smolina et al , 2016Roncalli et al 2016;Batta-Lona et al 2017). The genetic and genomic bases of such gene expression differences have received considerable attention (see review by Romero et al 2014).…”

Section: Genomic Basis Of Adaptationmentioning

confidence: 99%

Population Genomics of Marine Zooplankton

Bucklin

DiVito

Smolina

et al. 2018

Population Genomics

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The exceptionally large population size and cosmopolitan biogeographic distribution that distinguish many -but not all -marine zooplankton species generate similarly exceptional patterns of population genetic and genomic diversity and structure. The phylogenetic diversity of zooplankton has slowed the application of population genomic approaches, due to lack of genomic resources for closelyrelated species and diversity of genomic architecture, including highly-replicated genomes of many crustaceans. Use of numerous genomic markers, especially single nucleotide polymorphisms (SNPs), is transforming our ability to analyze population genetics and connectivity of marine zooplankton, and providing new understanding and different answers than earlier analyses, which typically used mitochondrial DNA and microsatellite markers. Population genomic approaches have confirmed that, despite high dispersal potential, many zooplankton species exhibit genetic structuring among geographic populations, especially at large ocean-basin scales, and have revealed patterns and pathways of population connectivity that do not always track ocean circulation. Genomic and transcriptomic resources are critically needed to allow further examination of micro-evolution and local adaptation, including identification of genes that show evidence of selection. These new tools will also enable further examination of the significance of small-scale genetic heterogeneity of marine zooplankton, to discriminate genetic "noise" in large and patchy populations from local adaptation to environmental conditions and change.

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Reduced up-regulation of gene expression in response to elevated temperatures in the mid-Atlantic population of Calanus finmarchicus

Cited by 5 publications

References 81 publications

Integrating patterns of thermal tolerance and phenotypic plasticity with population genetics to improve understanding of vulnerability to warming in a widespread copepod

Integrating patterns of thermal tolerance and phenotypic plasticity with population genetics to improve understanding of vulnerability to warming in a widespread copepod

Environmental Stress Responses and Experimental Handling Artifacts of a Model Organism, the Copepod Acartia tonsa (Dana)

Population Genomics of Marine Zooplankton

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