Transgenerational effects alleviate severe fecundity loss during ocean acidification in a ubiquitous planktonic copepod

Abstract

Ocean acidification (OA) caused by anthropogenic CO2 emission is projected for thousands of years to come, and significant effects are predicted for many marine organisms. While significant evolutionary responses are expected during such persistent environmental change, most studies consider only short-term effects. Little is known about the transgenerational effects of parental environments or natural selection on the capacity of populations to counter detrimental OA effects. In this study, six laboratory populations of the calanoid copepod Pseudocalanus acuspes were established at three different CO2 partial pressures (pCO2 of 400, 900 and 1550 μatm) and grown for two generations at these conditions. Our results show evidence of alleviation of OA effects as a result of transgenerational effects in P. acuspes. Second generation adults showed a 29% decrease in fecundity at 900 μatm CO2 compared to 400 μatm CO2 . This was accompanied by a 10% increase in metabolic rate indicative of metabolic stress. Reciprocal transplant tests demonstrated that this effect was reversible and the expression of phenotypic plasticity. Furthermore, these tests showed that at a pCO2 exceeding the natural range experienced by P. acuspes (1550 μatm), fecundity would have decreased by as much as 67% compared to at 400 μatm CO2 as a result of this plasticity. However, transgenerational effects partly reduced OA effects so that the loss of fecundity remained at a level comparable to that at 900 μatm CO2 . This also relieved the copepods from metabolic stress, and respiration rates were lower than at 900 μatm CO2 . These results highlight the importance of tests for transgenerational effects to avoid overestimation of the effects of OA.

Regulation of gene expression is associated with tolerance of the Arctic copepod Calanus glacialis to CO2‐acidified sea water

“…Indeed, epigenetic acclimation to stressors may be possible in copepods. Transgenerational effects (either adaptation or epigenetic acclimation) in the copepod Pseudocalanus acuspes alleviated the negative effect of low pH after two generations in low pH (Thor & Dupont, 2015). While the temporal duration of the chromatin modifications in C. glacialis at low pH, or their ability to be epigenetically passed on to the next generation, is unknown, they may play a part in both acclimatization within a single lifetime and over several generations.…”

“…Some species show no changes in development, respiration, and feeding rates with lowered pH (Kurihara & Ishimatsu, 2008; Mayor, Everett, & Cook, 2012; McConville et al., 2013; Runge, Fields, & Thompson, 2016), whereas other calanoid species are detrimentally affected (Zhang, Li, Wang, & Guo, 2011; Fitzer et al., 2012; Pedersen, Håkedal, & Salaberria, 2014; Thor & Dupont, 2015). Effects may vary by species, but also by life stage, with eggs and early naupliar stages being most vulnerable (Cripps, Lindeque, & Flynn, 2014; Pedersen, Våge, Olsen, Hammer, & Altin, 2014).…”

Species-specific responses to ocean acidification should account for local adaptation and adaptive plasticity

“…In addition, this environmental variability can drive associated local adaptation, which can also play a key role in setting sensitivity of a species to changes in pH/p CO2 . For example, the precise physiological 19,20 and evolutionary processes 21 involved can be different depending on whether experimental scenarios are within or outside of the natural range of variability experienced by that organism.…”

Can multi-generational exposure to ocean warming and acidification lead to the adaptation of life-history and physiology in a marine metazoan?

“…30% losses in aerobic scope in the damselfish Acanthochromis polyacanthus , while parental exposure to warming and acidification (+3°C and +600 µatm P CO2 ) prevented decreases in size, weight and survival in offspring of the anemonefish Amphiprion melanopus (Miller et al, 2012). The effects of parental conditioning are not confined to vertebrates; parental exposure to acidification (+1150 µatm P CO2 ) halved the reduction in fecundity caused by acute exposure to the same conditions in offspring of the copepod Pseudocalanus acuspes (Thor and Dupont, 2015), while parental exposure to ocean warming and acidification (+2°C and +400 µatm P CO2 ) reduced the negative effects of acute exposure on larval size in the coral Pocillopora damicornis . However, parental and acute exposure to combined global change drivers does not always affect the progeny, despite the negative effects of singlestressor exposure, as shown recently in the marine polychaete Ophryotroca labronica (Chakravarti et al, 2016).…”

“…In this respect, the selection pressures experienced by an individual's parents, grandparents, and the procession of generations before that, become crucial for determining the fitness and performance of future generations (Badyaev and Uller, 2009;Shama et al, 2016). Parental conditioning to global change drivers has largely positive effects on an offspring's response to the same stressor Miller et al, 2012;Salinas and Munch, 2012;Massamba N'Siala et al, 2014;Putnam and Gates, 2015;Rodríguez-Romero et al, 2016;Thor and Dupont, 2015). For example, parental exposure to warming (+3°C; all values are expressed relative to the control conditions) protected offspring from ca.…”