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Persistence of Positive Carryover Effects in the Oyster, Saccostrea glomerata, following Transgenerational Exposure to Ocean Acidification.

Parker LM, O'Connor WA, Raftos DA, Pörtner HO, Ross PM - PLoS ONE (2015)

Bottom Line: But whether these positive carryover effects can persist into adulthood or the next generation is unknown.We found that the capacity of adults to regulate extracellular pH at elevated CO2 was improved if they had a prior history of transgenerational exposure to elevated CO2.Offspring with a history of transgenerational exposure to elevated CO2 had a lower percentage abnormality, faster development rate, faster shell growth and increased heart rate at elevated CO2 compared with F2 offspring with no prior history of exposure to elevated CO2.

View Article: PubMed Central - PubMed

Affiliation: School of Science and Health, University of Western Sydney, Hawkesbury K12, Locked Bag 1797, Penrith South DC 2751, Sydney, New South Wales, Australia.

ABSTRACT
Ocean acidification (OA) is predicted to have widespread implications for marine organisms, yet the capacity for species to acclimate or adapt over this century remains unknown. Recent transgenerational studies have shown that for some marine species, exposure of adults to OA can facilitate positive carryover effects to their larval and juvenile offspring that help them to survive in acidifying oceanic conditions. But whether these positive carryover effects can persist into adulthood or the next generation is unknown. Here we tested whether positive carryover effects found in larvae of the oyster, Saccostrea glomerata following transgenerational exposure to elevated CO2, could persist into adulthood and whether subsequent transgenerational exposure of adults to elevated CO2 would facilitate similar adaptive responses in the next generation of larvae and juveniles. Following our previous transgenerational exposure of parental adults and first generation (F1) larvae to ambient (385 μatm) and elevated (856 μatm) CO2, newly settled F1 juveniles were transferred to the field at ambient CO2 for 14 months, until they reached reproductive maturity. At this time, the F1 adults were returned to the laboratory and the previous transgenerational CO2 exposure was repeated to produce F2 offspring. We found that the capacity of adults to regulate extracellular pH at elevated CO2 was improved if they had a prior history of transgenerational exposure to elevated CO2. In addition, subsequent transgenerational exposure of these adults led to an increase in the resilience of their larval and juvenile offspring. Offspring with a history of transgenerational exposure to elevated CO2 had a lower percentage abnormality, faster development rate, faster shell growth and increased heart rate at elevated CO2 compared with F2 offspring with no prior history of exposure to elevated CO2. Our results suggest that positive carryover effects originating during parental and larval exposure will be important in mediating some of the impacts of OA for later life-history stages and generations.

No MeSH data available.


Related in: MedlinePlus

Flow chart of the experimental design.X indicates that these lines were not followed through to the F2 generation.
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pone.0132276.g001: Flow chart of the experimental design.X indicates that these lines were not followed through to the F2 generation.

Mentions: For detailed information on the first transgenerational exposure (Parental generation adults to F1 larvae) see Parker et al. [5]. Briefly, following the 2 w acclimation period, parental generation adults were divided at random into 6 groups of 50 oysters. Each group was transferred into a separate 40 L tub supplied by its own 750 L header tank. Three of the header tanks were set at ambient CO2 of 385 μatm while the other three were set at elevated CO2 of 856 μatm. Adults were fed the same combined algal diet provided during their acclimation period. Complete water changes were made every 2 d using preequilibrated filtered seawater (FSW) and oysters were briefly removed out of water each day (10 seconds) and rinsed with freshwater to remove faecal matter. Following 5 w of conditioning in the treatments the adults reached gravid stage and were strip spawned to allow the collection of eggs and sperm. Eggs and sperm from a minimum of 10 females and 10 males from each ‘parental adult CO2 treatment’ (ambient or elevated CO2) were filtered to remove debris and were fertilised in 20 L buckets at the same CO2 level that the adults were held at (FSW, 24°C, salinity 34.6 ppt). The gametes were allowed to fertilise for 30 min to create two F1 offspring lines: ambient parental adult exposure, ambient F1 larval exposure (referred to here after as the ‘F1-control line’); and elevated parental adult exposure, elevated F1 larval exposure (referred to here after as the ‘F1-transgen line’). Following fertilisation the embryos from each line were transferred into 200 L polyethylene larval rearing tanks held at the same CO2 concentration that they were fertilised in. There were three replicates for each of the two offspring lines (Fig 1). Larval feeding began after 16 h with the appearance of the first D-veliger larval stage. Larvae were fed an algal diet twice daily consisting of 50% Chaetoceros calcitrans, 25% P. lutheri and 25% T. Isochrysis aff. galbana for the first week of development [27]. After this time, C. calcitrans was gradually replaced with C. muelleri as the larvae increased in size. Algal concentrations ranged from 1 x 104 cells mL-1 at the beginning of the larval experiment up to 1.16 x 105 cells mL-1 at the completion of the larval experiment. Once the larvae reached eyed stage and showed signs of settlement (eye spot, 300 μm shell length, protruding foot, crawling, approximately 19 d– 21 d depending on the larval and adult CO2 exposure treatment; see O’Connor et al. [27]) each replicate line was dosed with epinephrine (60 mg epinephrine per 2.5 g of larvae in 1 L FSW) to help induce settlement and were suspended on a 180 μm mesh settlement screen [27]. This is a common practice used in the hatchery production of this species [27]. To ensure maximum settlement and representation of each line, this process was repeated every 2 d for 6 d. Newly settled juvenile spat were rinsed with freshwater and brushed gently daily to prevent them from settling on the screens.


Persistence of Positive Carryover Effects in the Oyster, Saccostrea glomerata, following Transgenerational Exposure to Ocean Acidification.

Parker LM, O'Connor WA, Raftos DA, Pörtner HO, Ross PM - PLoS ONE (2015)

Flow chart of the experimental design.X indicates that these lines were not followed through to the F2 generation.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4493068&req=5

pone.0132276.g001: Flow chart of the experimental design.X indicates that these lines were not followed through to the F2 generation.
Mentions: For detailed information on the first transgenerational exposure (Parental generation adults to F1 larvae) see Parker et al. [5]. Briefly, following the 2 w acclimation period, parental generation adults were divided at random into 6 groups of 50 oysters. Each group was transferred into a separate 40 L tub supplied by its own 750 L header tank. Three of the header tanks were set at ambient CO2 of 385 μatm while the other three were set at elevated CO2 of 856 μatm. Adults were fed the same combined algal diet provided during their acclimation period. Complete water changes were made every 2 d using preequilibrated filtered seawater (FSW) and oysters were briefly removed out of water each day (10 seconds) and rinsed with freshwater to remove faecal matter. Following 5 w of conditioning in the treatments the adults reached gravid stage and were strip spawned to allow the collection of eggs and sperm. Eggs and sperm from a minimum of 10 females and 10 males from each ‘parental adult CO2 treatment’ (ambient or elevated CO2) were filtered to remove debris and were fertilised in 20 L buckets at the same CO2 level that the adults were held at (FSW, 24°C, salinity 34.6 ppt). The gametes were allowed to fertilise for 30 min to create two F1 offspring lines: ambient parental adult exposure, ambient F1 larval exposure (referred to here after as the ‘F1-control line’); and elevated parental adult exposure, elevated F1 larval exposure (referred to here after as the ‘F1-transgen line’). Following fertilisation the embryos from each line were transferred into 200 L polyethylene larval rearing tanks held at the same CO2 concentration that they were fertilised in. There were three replicates for each of the two offspring lines (Fig 1). Larval feeding began after 16 h with the appearance of the first D-veliger larval stage. Larvae were fed an algal diet twice daily consisting of 50% Chaetoceros calcitrans, 25% P. lutheri and 25% T. Isochrysis aff. galbana for the first week of development [27]. After this time, C. calcitrans was gradually replaced with C. muelleri as the larvae increased in size. Algal concentrations ranged from 1 x 104 cells mL-1 at the beginning of the larval experiment up to 1.16 x 105 cells mL-1 at the completion of the larval experiment. Once the larvae reached eyed stage and showed signs of settlement (eye spot, 300 μm shell length, protruding foot, crawling, approximately 19 d– 21 d depending on the larval and adult CO2 exposure treatment; see O’Connor et al. [27]) each replicate line was dosed with epinephrine (60 mg epinephrine per 2.5 g of larvae in 1 L FSW) to help induce settlement and were suspended on a 180 μm mesh settlement screen [27]. This is a common practice used in the hatchery production of this species [27]. To ensure maximum settlement and representation of each line, this process was repeated every 2 d for 6 d. Newly settled juvenile spat were rinsed with freshwater and brushed gently daily to prevent them from settling on the screens.

Bottom Line: But whether these positive carryover effects can persist into adulthood or the next generation is unknown.We found that the capacity of adults to regulate extracellular pH at elevated CO2 was improved if they had a prior history of transgenerational exposure to elevated CO2.Offspring with a history of transgenerational exposure to elevated CO2 had a lower percentage abnormality, faster development rate, faster shell growth and increased heart rate at elevated CO2 compared with F2 offspring with no prior history of exposure to elevated CO2.

View Article: PubMed Central - PubMed

Affiliation: School of Science and Health, University of Western Sydney, Hawkesbury K12, Locked Bag 1797, Penrith South DC 2751, Sydney, New South Wales, Australia.

ABSTRACT
Ocean acidification (OA) is predicted to have widespread implications for marine organisms, yet the capacity for species to acclimate or adapt over this century remains unknown. Recent transgenerational studies have shown that for some marine species, exposure of adults to OA can facilitate positive carryover effects to their larval and juvenile offspring that help them to survive in acidifying oceanic conditions. But whether these positive carryover effects can persist into adulthood or the next generation is unknown. Here we tested whether positive carryover effects found in larvae of the oyster, Saccostrea glomerata following transgenerational exposure to elevated CO2, could persist into adulthood and whether subsequent transgenerational exposure of adults to elevated CO2 would facilitate similar adaptive responses in the next generation of larvae and juveniles. Following our previous transgenerational exposure of parental adults and first generation (F1) larvae to ambient (385 μatm) and elevated (856 μatm) CO2, newly settled F1 juveniles were transferred to the field at ambient CO2 for 14 months, until they reached reproductive maturity. At this time, the F1 adults were returned to the laboratory and the previous transgenerational CO2 exposure was repeated to produce F2 offspring. We found that the capacity of adults to regulate extracellular pH at elevated CO2 was improved if they had a prior history of transgenerational exposure to elevated CO2. In addition, subsequent transgenerational exposure of these adults led to an increase in the resilience of their larval and juvenile offspring. Offspring with a history of transgenerational exposure to elevated CO2 had a lower percentage abnormality, faster development rate, faster shell growth and increased heart rate at elevated CO2 compared with F2 offspring with no prior history of exposure to elevated CO2. Our results suggest that positive carryover effects originating during parental and larval exposure will be important in mediating some of the impacts of OA for later life-history stages and generations.

No MeSH data available.


Related in: MedlinePlus