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Diversification, evolution and sub-functionalization of 70kDa heat-shock proteins in two sister species of antarctic krill: differences in thermal habitats, responses and implications under climate change.

Cascella K, Jollivet D, Papot C, Léger N, Corre E, Ravaux J, Clark MS, Toullec JY - PLoS ONE (2015)

Bottom Line: They therefore provide a useful model system for the investigation of adaptations to thermal tolerance.Initial CTmax studies showed that E. superba was slightly more thermotolerant than E. crystallorophias.Furthermore, analyses conducted to estimate the evolutionary rates and selection strengths acting on each gene tended to support the hypothesis that diversifying selection has contributed to the diversification of this gene family, and led to the selective relaxation on the inducible C form with its possible loss of function in the two krill species.

View Article: PubMed Central - PubMed

Affiliation: Sorbonne Universités, UPMC Université Paris 06, UMR 7144 CNRS, Equipe ABICE, Station Biologique de Roscoff, 29680 Roscoff, France; CNRS, UMR 7144, Adaptation et Diversité en Milieu Marin, Station Biologique de Roscoff, 29680 Roscoff, France.

ABSTRACT

Background: A comparative thermal tolerance study was undertaken on two sister species of Euphausiids (Antarctic krills) Euphausia superba and Euphausia crystallorophias. Both are essential components of the Southern Ocean ecosystem, but occupy distinct environmental geographical locations with slightly different temperature regimes. They therefore provide a useful model system for the investigation of adaptations to thermal tolerance.

Methodology/principal finding: Initial CTmax studies showed that E. superba was slightly more thermotolerant than E. crystallorophias. Five Hsp70 mRNAs were characterized from the RNAseq data of both species and subsequent expression kinetics studies revealed notable differences in induction of each of the 5 orthologues between the two species, with E. crystallorophias reacting more rapidly than E. superba. Furthermore, analyses conducted to estimate the evolutionary rates and selection strengths acting on each gene tended to support the hypothesis that diversifying selection has contributed to the diversification of this gene family, and led to the selective relaxation on the inducible C form with its possible loss of function in the two krill species.

Conclusions: The sensitivity of the epipelagic species E. crystallorophias to temperature variations and/or its adaptation to cold is enhanced when compared with its sister species, E. superba. These results indicate that ice krill could be the first of the two species to be impacted by the warming of coastal waters of the Austral ocean in the coming years due to climate change.

No MeSH data available.


Related in: MedlinePlus

Curves representing the loss of mobility of a population of krill subjected to gradual temperature increase (0.1.min-1) (E. crystallorophias n = 130 blue curve; E. superba n = 43 red curve).CTmax is the temperature at which 50% of mobile animals are reached.
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pone.0121642.g001: Curves representing the loss of mobility of a population of krill subjected to gradual temperature increase (0.1.min-1) (E. crystallorophias n = 130 blue curve; E. superba n = 43 red curve).CTmax is the temperature at which 50% of mobile animals are reached.

Mentions: As a preliminary analysis to understand the thermal resilience of E. superba and E. crystallorophias in the Southern Ocean, short term acute exposures were undertaken, using a temperature increase of 0.1°C/min. The interpretation of the CTmax curves of the two species (Fig. 1) gives values for E. superba and E. crystallorophias of 15.8 ±0.1°C and 14.7 ± 0.1°C respectively. These temperatures indicate that these two species of krill may be some of the most thermotolerant invertebrates in the Southern Ocean [36–38]. These animals are particularly mobile, (pelagic and epi-pelagic) and whilst most measures to date have been carried out on benthic animals, studies have shown mobility to significantly correlate with thermal tolerance under rapid thermal challenges [38]. Whilst the thermal shocks applied here are relatively short and represent very rapid temperature increases, longer term experiments, especially for pelagic species, such as krill are difficult to put in place without a specialised facility and detailed knowledge of long-term husbandry, however, such short term studies can be used to extrapolate predictions for longer term survival [38]. There was an additional observation with this experiment, which may indicate that behaviour may also impact on the thermal response of these species. All animals for the experiments were taken from the upper water column of the stock aquarium ensuring that they were active swimmers, but there was an interesting difference in response between the two species. Despite the small difference in CTmax (1°C) between these two species, E. superba appeared to maintain a superior swimming capacity during the experiment. When the water temperature was only raised to 2°C, the ice krill response was characterised by swimming along the bottom (S1 Fig.). This may have been due either to a reduction in capacity indicated by a loss of swimming activity or simply a escape response to keep as deep as possible in the face of this environmental challenge [39,40].


Diversification, evolution and sub-functionalization of 70kDa heat-shock proteins in two sister species of antarctic krill: differences in thermal habitats, responses and implications under climate change.

Cascella K, Jollivet D, Papot C, Léger N, Corre E, Ravaux J, Clark MS, Toullec JY - PLoS ONE (2015)

Curves representing the loss of mobility of a population of krill subjected to gradual temperature increase (0.1.min-1) (E. crystallorophias n = 130 blue curve; E. superba n = 43 red curve).CTmax is the temperature at which 50% of mobile animals are reached.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4383606&req=5

pone.0121642.g001: Curves representing the loss of mobility of a population of krill subjected to gradual temperature increase (0.1.min-1) (E. crystallorophias n = 130 blue curve; E. superba n = 43 red curve).CTmax is the temperature at which 50% of mobile animals are reached.
Mentions: As a preliminary analysis to understand the thermal resilience of E. superba and E. crystallorophias in the Southern Ocean, short term acute exposures were undertaken, using a temperature increase of 0.1°C/min. The interpretation of the CTmax curves of the two species (Fig. 1) gives values for E. superba and E. crystallorophias of 15.8 ±0.1°C and 14.7 ± 0.1°C respectively. These temperatures indicate that these two species of krill may be some of the most thermotolerant invertebrates in the Southern Ocean [36–38]. These animals are particularly mobile, (pelagic and epi-pelagic) and whilst most measures to date have been carried out on benthic animals, studies have shown mobility to significantly correlate with thermal tolerance under rapid thermal challenges [38]. Whilst the thermal shocks applied here are relatively short and represent very rapid temperature increases, longer term experiments, especially for pelagic species, such as krill are difficult to put in place without a specialised facility and detailed knowledge of long-term husbandry, however, such short term studies can be used to extrapolate predictions for longer term survival [38]. There was an additional observation with this experiment, which may indicate that behaviour may also impact on the thermal response of these species. All animals for the experiments were taken from the upper water column of the stock aquarium ensuring that they were active swimmers, but there was an interesting difference in response between the two species. Despite the small difference in CTmax (1°C) between these two species, E. superba appeared to maintain a superior swimming capacity during the experiment. When the water temperature was only raised to 2°C, the ice krill response was characterised by swimming along the bottom (S1 Fig.). This may have been due either to a reduction in capacity indicated by a loss of swimming activity or simply a escape response to keep as deep as possible in the face of this environmental challenge [39,40].

Bottom Line: They therefore provide a useful model system for the investigation of adaptations to thermal tolerance.Initial CTmax studies showed that E. superba was slightly more thermotolerant than E. crystallorophias.Furthermore, analyses conducted to estimate the evolutionary rates and selection strengths acting on each gene tended to support the hypothesis that diversifying selection has contributed to the diversification of this gene family, and led to the selective relaxation on the inducible C form with its possible loss of function in the two krill species.

View Article: PubMed Central - PubMed

Affiliation: Sorbonne Universités, UPMC Université Paris 06, UMR 7144 CNRS, Equipe ABICE, Station Biologique de Roscoff, 29680 Roscoff, France; CNRS, UMR 7144, Adaptation et Diversité en Milieu Marin, Station Biologique de Roscoff, 29680 Roscoff, France.

ABSTRACT

Background: A comparative thermal tolerance study was undertaken on two sister species of Euphausiids (Antarctic krills) Euphausia superba and Euphausia crystallorophias. Both are essential components of the Southern Ocean ecosystem, but occupy distinct environmental geographical locations with slightly different temperature regimes. They therefore provide a useful model system for the investigation of adaptations to thermal tolerance.

Methodology/principal finding: Initial CTmax studies showed that E. superba was slightly more thermotolerant than E. crystallorophias. Five Hsp70 mRNAs were characterized from the RNAseq data of both species and subsequent expression kinetics studies revealed notable differences in induction of each of the 5 orthologues between the two species, with E. crystallorophias reacting more rapidly than E. superba. Furthermore, analyses conducted to estimate the evolutionary rates and selection strengths acting on each gene tended to support the hypothesis that diversifying selection has contributed to the diversification of this gene family, and led to the selective relaxation on the inducible C form with its possible loss of function in the two krill species.

Conclusions: The sensitivity of the epipelagic species E. crystallorophias to temperature variations and/or its adaptation to cold is enhanced when compared with its sister species, E. superba. These results indicate that ice krill could be the first of the two species to be impacted by the warming of coastal waters of the Austral ocean in the coming years due to climate change.

No MeSH data available.


Related in: MedlinePlus