Integrating laboratory experiments and biogeographic modelling approaches to understand sensitivity to ocean warming in rare and common marine annelids.

Among ectotherms, rare species are expected to have a narrower thermal niche breadth and reduced acclimation capacity and thus be more vulnerable to global warming than their common relatives. To assess these hypotheses, we experimentally quantified the thermal sensitivity of seven common, uncommon, and rare species of temperate marine annelids of the genus Ophryotrocha to assess their vulnerability to ocean warming. We measured the upper and lower limits of physiological thermal tolerance, survival, and reproductive performance of each species along a temperature gradient (18, 24, and 30 °C). We then combined this information to produce curves of each species' fundamental thermal niche by including trait plasticity. Each thermal curve was then expressed as a habitat suitability index (HSI) and projected for the Mediterranean Sea and temperate Atlantic Ocean under a present day (1970-2000), mid- (2050-2059) and late- (2090-2099) 21st Century scenario for two climate change scenarios (RCP2.6 and RCP8.5). Rare and uncommon species showed a reduced upper thermal tolerance compared to common species, and the niche breadth and acclimation capacity were comparable among groups. The simulations predicted an overall increase in the HSI for all species and identified potential hotspots of HSI decline for uncommon and rare species along the warm boundaries of their potential distribution, though they failed to project the higher sensitivity of these species into a greater vulnerability to ocean warming. In the discussion, we provide some caveats on the implications of our results for conservation efforts.

Plastic adjustments of biparental care behavior across embryonic development under elevated temperature in a marine ectotherm.

Phenotypic plasticity in parental care investment allows organisms to promptly respond to rapid environmental changes by potentially benefiting offspring survival and thus parental fitness. To date, a knowledge gap exists on whether plasticity in parental care behaviors can mediate responses to climate change in marine ectotherms. Here, we assessed the plasticity of parental care investment under elevated temperatures in a gonochoric marine annelid with biparental care, Ophryotrocha labronica, and investigated its role in maintaining the reproductive success of this species in a warming ocean. We measured the time individuals spent carrying out parental care activities across three phases of embryonic development, as well as the hatching success of the offspring as a proxy for reproductive success, at control (24℃) and elevated (27℃) temperature conditions. Under elevated temperature, we observed: (a) a significant decrease in total parental care activity, underpinned by a decreased in male and simultaneous parental care activity, in the late stage of embryonic development; and (b) a reduction in hatching success that was however not significantly related to changes in parental care activity levels. These findings, along with the observed unaltered somatic growth of parents and decreased brood size, suggest that potential cost-benefit trade-offs between offspring survival (i.e., immediate fitness) and parents' somatic condition (i.e., longer-term fitness potential) may occur under ongoing ocean warming. Finally, our results suggest that plasticity in parental care behavior is a mechanism able to partially mitigate the negative effects of temperature-dependent impacts.

Extensive gene rearrangements in the mitogenomes of congeneric annelid species and insights on the evolutionary history of the genus Ophryotrocha.

BACKGROUND: Annelids are one the most speciose and ecologically diverse groups of metazoans. Although a significant effort has been recently invested in sequencing genomes of a wide array of metazoans, many orders and families within the phylum Annelida are still represented by a single specimen of a single species. The genus of interstitial annelids Ophryotrocha (Dorvilleidae, Errantia, Annelida) is among these neglected groups, despite its extensive use as model organism in numerous studies on the evolution of life history, physiological and ecological traits. To compensate for the paucity of genomic information in this genus, we here obtained novel complete mitochondrial genomes of six Ophryotrocha species using next generation sequencing. In addition, we investigated the evolution of the reproductive mode in the Ophryotrocha genus using a phylogeny based on two mitochondrial markers (COXI and 16S rDNA) and one nuclear fragment (Histone H3). RESULTS: Surprisingly, gene order was not conserved among the six Ophryotrocha species investigated, and varied greatly as compared to those found in other annelid species within the class Errantia. The mitogenome phylogeny for the six Ophryotrocha species displayed a separation of gonochoric and hermaphroditic species. However, this separation was not observed in the phylogeny based on the COX1, 16S rDNA, and H3 genes. Parsimony and Bayesian ancestral trait reconstruction indicated that gonochorism was the most parsimonious ancestral reproductive mode in Ophryotrocha spp. CONCLUSIONS: Our results highlight the remarkably high level of gene order variation among congeneric species, even in annelids. This encourages the need for additional mitogenome sequencing of annelid taxa in order to properly understand its mtDNA evolution, high biodiversity and phylogenetic relationships.

Life-history trade-offs and limitations associated with phenotypic adaptation under future ocean warming and elevated salinity.

Little is known about the life-history trade-offs and limitations, and the physiological mechanisms that are associated with phenotypic adaptation to future ocean conditions. To address this knowledge gap, we investigated the within- and trans-generation life-history responses and aerobic capacity of a marine polychaete, Ophryotrocha labronica, to elevated temperature and elevated temperature combined with elevated salinity for its entire lifespan. In addition, transplants between treatments were carried out at both the egg mass and juvenile stage to identify the potential influence of developmental effects. Within-generation, life-history trade-offs caused by the timing of transplant were only detected under elevated temperature combined with elevated salinity conditions. Polychaetes transplanted at the egg mass stage grew slower and had lower activities of energy metabolism enzymes but reached a larger maximum body size and lived longer when compared with those transplanted as juveniles. Trans-generation exposure to both elevated temperature and elevated temperature and salinity conditions restored 20 and 21% of lifespan fecundity, respectively. Trans-generation exposure to elevated temperature conditions also resulted in a trade-off between juvenile growth rates and lifespan fecundity, with slower growers showing greater fecundity. Overall, our results suggest that future ocean conditions may select for slower growers. Furthermore, our results indicate that life-history trade-offs and limitations will be more prevalent with the shift of multiple global change drivers, and thus there will be greater constraints on adaptive potential. This article is part of the theme issue 'The role of plasticity in phenotypic adaptation to rapid environmental change'.

The evolution of phenotypic plasticity under global change.

Marine ecosystems are currently in a state of flux, with ocean warming and acidification occurring at unprecedented rates. Phenotypic plasticity underpins acclimatory responses by shifting the mean phenotype in a population, which may buffer the negative effects of global change. However, little is known about how phenotypic plasticity evolves across multiple generations. We tested this by reciprocally-transplanting the polychaete Ophryotrocha labronica between control and global change scenarios (ocean warming and acidification in isolation and combined) over five generations. By comparing the reaction norms of four life-history traits across generations, we show that juvenile developmental rate in the combined scenario was the only trait that changed its plastic response across generations when transplanted back to control conditions, and that adaptive plasticity was conserved in most traits, despite significant levels of selection and strong declines in individual fitness in the multi-generational exposure. We suggest the change in level of plasticity in the combined scenario is caused by differential allocation of energy between the mean and the plasticity of the trait along the multigenerational exposure. The ability to maintain within-generational levels of plasticity under global change scenarios has important eco-evolutionary and conservation implications, which are examined under the framework of assisted evolution programs.

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

Ocean warming and acidification are concomitant global drivers that are currently threatening the survival of marine organisms. How species will respond to these changes depends on their capacity for plastic and adaptive responses. Little is known about the mechanisms that govern plasticity and adaptability or how global changes will influence these relationships across multiple generations. Here, we exposed the emerging model marine polychaete Ophryotrocha labronica to conditions simulating ocean warming and acidification, in isolation and in combination over five generations to identify: (i) how multiple versus single global change drivers alter both juvenile and adult life-history traits; (ii) the mechanistic link between adult physiological and fitness-related life-history traits; and (iii) whether the phenotypic changes observed over multiple generations are of plastic and/or adaptive origin. Two juvenile (developmental rate; survival to sexual maturity) and two adult (average reproductive body size; fecundity) life-history traits were measured in each generation, in addition to three physiological (cellular reactive oxygen species content, mitochondrial density, mitochondrial capacity) traits. We found that multi-generational exposure to warming alone caused an increase in juvenile developmental rate, reactive oxygen species production and mitochondrial density, decreases in average reproductive body size and fecundity, and fluctuations in mitochondrial capacity, relative to control conditions. Exposure to ocean acidification alone had only minor effects on juvenile developmental rate. Remarkably, when both drivers of global change were present, only mitochondrial capacity was significantly affected, suggesting that ocean warming and acidification act as opposing vectors of stress across multiple generations.

Multi-generational responses of a marine polychaete to a rapid change in seawater pCO2.

Little is known of the capacity that marine metazoans have to evolve under rapid p CO 2 changes. Consequently, we reared a marine polychaete, Ophryotrocha labronica, previously cultured for approximately 33 generations under a low/variable pH regime, under elevated and low p CO 2 for six generations. The strain used was found to be tolerant to elevated p CO 2 conditions. In generations F1 and F2 females' fecundity was significantly lower in the low p CO 2 treatment. However, from generation F3 onwards there were no differences between p CO 2 treatments, indicating that trans-generational effects enabled the restoration and maintenance of reproductive output. Whilst the initial fitness recovery was likely driven by trans-generational plasticity (TGP), the results from reciprocal transplant assays, performed using F7 individuals, made it difficult to disentangle between whether TGP had persisted across multiple generations, or if evolutionary adaptation had occurred. Nonetheless, both are important mechanisms for persistence under climate change. Overall, our study highlights the importance of multi-generational experiments in more accurately determining marine metazoans' responses to changes in p CO 2, and strengthens the case for exploring their use in conservation, by creating specific p CO 2 tolerant strains of keystone ecosystem species.

Can trans-generational experiments be used to enhance species resilience to ocean warming and acidification?

Human-assisted, trans-generational exposure to ocean warming and acidification has been proposed as a conservation and/or restoration tool to produce resilient offspring. To improve our understanding of the need for and the efficacy of this approach, we characterized life-history and physiological responses in offspring of the marine polychaete Ophryotrocha labronica exposed to predicted ocean warming (OW: + 3°C), ocean acidification (OA: pH -0.5) and their combination (OWA: + 3°C, pH -0.5), following the exposure of their parents to either control conditions (within-generational exposure) or the same conditions (trans-generational exposure). Trans-generational exposure to OW fully alleviated the negative effects of within-generational exposure to OW on fecundity and egg volume and was accompanied by increased metabolic activity. While within-generational exposure to OA reduced juvenile growth rates and egg volume, trans-generational exposure alleviated the former but could not restore the latter. Surprisingly, exposure to OWA had no negative impacts within- or trans-generationally. Our results highlight the potential for trans-generational laboratory experiments in producing offspring that are resilient to OW and OA. However, trans-generational exposure does not always appear to improve traits and therefore may not be a universally useful tool for all species in the face of global change.

Trans-generational plasticity in physiological thermal tolerance is modulated by maternal pre-reproductive environment in the polychaete Ophryotrocha labronica.

Maternal temperature is known to affect many aspects of offspring phenotype, but its effect on offspring physiological thermal tolerance has received less attention, despite the importance of physiological traits in defining organismal ability to cope with temperature changes. To fill this gap, we used the marine polychaete Ophryotrocha labronica to investigate the influence of maternal temperature on offspring upper and lower thermal tolerance limits, and assess whether maternal influence changed according to the stage of offspring pre-zygotic development at which a thermal cue was provided. Measurements were taken on adult offspring acclimated to 18 or 30°C, produced by mothers previously reared at 24°C and then exposed to 18 or 30°C at an early and late stage of oogenesis. When the shift from 24°C was provided early during oogenesis, mothers produced offspring with greater cold and heat tolerance whenever mother-offspring temperatures did not match, with respect to when they matched, suggesting the presence of an anticipatory maternal effect triggered by the thermal variation. Conversely, when the cue was provided later during oogenesis, more tolerant offspring were observed when temperatures persisted across generations. In this case, maternal exposure to 18 or 30°C may have benefited offspring performance, while limitations in the transmission of the thermal cue may account for the lack of correlation between maternal experiences and offspring performance when mother-offspring environments did not match. Our results provided evidence for a trans-generational effect of temperature on physiological performance characterised by a high context dependency, and are discussed in the light of maternal pre-reproductive experiences.