Will life find a way? Evolution of marine species under global change

Projections of marine biodiversity and implementation of effective actions for its maintenance in the face of current rapid global environmental change are constrained by our limited understanding of species’ adaptive responses, including transgenerational plasticity, epigenetics and natural selection. This special issue presents 13 novel studies, which employ experimental and modelling approaches to (i) investigate plastic and evolutionary responses of marine species to major global change drivers; (ii) ask relevant broad eco-evolutionary questions, implementing multiple species and populations studies; (iii) show the advantages of using advanced experimental designs and tools; (iv) construct novel model organisms for marine evolution; (v) help identifying future challenges for the field; and (vi) highlight the importance of incorporating existing evolutionary theory into management solutions for the marine realm. What emerges is that at least some populations of marine species have the ability to adapt to future global change conditions. However, marine organisms’ capacity for adaptation appears finite, due to evolutionary trade-offs and possible rapid losses in genetic diversity. This further corroborates the idea that acquiring an evolutionary perspective on how marine life will respond to the selective pressure of future global changes will guide us in better identifying which conservation efforts will be most needed and most effective

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

Long-term exposure to elevated pCO2 more than warming modifies juvenile shell growth patterns in a temperate gastropod

Co-occurring global change drivers, such as ocean warming and acidification, can have large impacts on the behaviour, physiology, and health of marine organisms. However, whilst early-life stages are thought to be most sensitive to these impacts, little is known about the individual level processes by which such impacts take place. Here, using mesocosm experiments simulating ocean warming (OW) and ocean acidification (OA) conditions expected for the NE Atlantic region by 2100 using a variety of treatments of elevated pCO2 and temperature. We investigated their impacts on bio-mineralization, microstructure, and ontogeny of Nucella lapillus (L.) juveniles, a common gastropod predator that exerts important top-down controls on biodiversity patterns in temperate rocky shores. The shell of juveniles hatched in mesocosms during a 14 month long experiment were analysed using micro-CT scanning, 3D geometric morphometrics, and scanning-electron microscopy. Elevated temperature and age determined shell density, length, width, thickness, elemental chemistry, shape, and shell surface damages. However, co-occurring elevated pCO2 modified the impacts of elevated temperature, in line with expected changes in carbonate chemistry driven by temperature. Young N. lapillus from acidified treatments had weaker shells and were therefore expected to be more vulnerable to predation and environmental pressures such as wave action. However, in some instances, the effects of both higher CO2 content and elevated temperature appeared to have reversed as the individuals aged. This study suggests that compensatory development may therefore occur, and that expected increases in juvenile mortality under OA and OW may be counteracted, to some degree, by high plasticity in shell formation in this species. This feature may prove advantageous for N. lapillus community dynamics in near-future conditions

An in situ assessment of local adaptation in a calcifying polychaete from a shallow CO 2 vent system

Ocean acidification (OA) is likely to exert selective pressure on natural populations. Our ability to predict which marine species will adapt to OA and what underlies this adaptive potential is of high conservation and resource management priority. Using a naturally low-pH vent site in the Mediterranean Sea (Castello Aragonese, Ischia) mirroring projected future OA conditions, we carried out a reciprocal transplant experiment to investigate the relative importance of phenotypic plasticity and local adaptation in two populations of the sessile, calcifying polychaete Simplaria sp. (Annelida, Serpulidae, Spirorbinae): one residing in low pH and the other from a nearby ambient (i.e. high) pH site. We measured a suite of fitness-related traits (i.e. survival, reproductive output, maturation, population growth) and tube growth rates in laboratory-bred F2 generation individuals from both populations reciprocally transplanted back into both ambient and low-pH in situ habitats. Both populations showed lower expression in all traits, but increased tube growth rates, when exposed to low-pH compared with high-pH conditions, regardless of their site of origin suggesting that local adaptation to low-pH conditions has not occurred. We also found comparable levels of plasticity in the two populations investigated, suggesting no influence of long-term exposure to low pH on the ability of populations to adjust their phenotype. Despite high variation in trait values among sites and the relatively extreme conditions at the low pH site (pH < 7.36), response trends were consistent across traits. Hence, our data suggest that, for Simplaria and possibly other calcifiers, neither local adaptations nor sufficient phenotypic plasticity levels appear to suffice in order to compensate for the negative impacts of OA on long-term survival. Our work also emphasizes the utility of field experiments in natural environments subjected to high level of pCO2 for elucidating the potential for adaptation to future scenarios of OA

Adaptation and acclimatization to ocean acidification in marine ectotherms: an in situ transplant experiment with polychaetes at a shallow CO₂ vent system

Metabolic rate determines the physiological and life-history performances of ectotherms. Thus, the extent to which such rates are sensitive and plastic to environmental perturbation is central to an organism's ability to function in a changing environment. Little is known of long-term metabolic plasticity and potential for metabolic adaptation in marine ectotherms exposed to elevated pCO₂. Consequently, we carried out a series of in situ transplant experiments using a number of tolerant and sensitive polychaete species living around a natural CO₂ vent system. Here, we show that a marine metazoan (i.e. Platynereis dumerilii) was able to adapt to chronic and elevated levels of pCO₂. The vent population of P. dumerilii was physiologically and genetically different from nearby populations that experience low pCO₂, as well as smaller in body size. By contrast, different populations of Amphiglena mediterranea showed marked physiological plasticity indicating that adaptation or acclimatization are both viable strategies for the successful colonization of elevated pCO₂ environments. In addition, sensitive species showed either a reduced or increased metabolism when exposed acutely to elevated pCO₂. Our findings may help explain, from a metabolic perspective, the occurrence of past mass extinction, as well as shed light on alternative pathways of resilience in species facing ongoing ocean acidification

Does plasticity in thermal tolerance trade off with inherent tolerance? The influence of setal tracheal gills on thermal tolerance and its plasticity in a group of European diving beetles.

In the face of global warming, both the absolute thermal tolerance of an ectotherms, and its ability to shift its tolerance level via acclimation, are thought to be fundamentally important. Understanding the links between tolerance and its plasticity is therefore critical to accurately predict vulnerability to warming. Previous studies in a number of ectotherm taxa suggest trade-offs in the evolution of thermal tolerance and its plasticity, something which does not, however, apply to Deronectes diving beetles, where these traits are instead positively correlated. Here we revisit the relationship between thermal tolerance and plasticity in these beetles, paying attention to a recently discovered morphological adaptation supporting under water respiration - setal tracheal gills. Hollow setae on the elytra interconnect with the beetle's tracheal system, providing a gas exchange surface that allows oxygen to be extracted directly from the water. This enables individuals to stay submerged for longer than their subelytral air stores would allow. We show that hypoxia reduced heat tolerance, especially when individuals were denied access to air, forcing them to rely solely on aquatic gas exchange. Species with higher densities of these gas-exchanging setae exhibited improved cold tolerance, but reduced heat tolerance and lower plasticity of heat tolerance. Differences in setal tracheal gill density across species were also related to habitat use: species with low gill density were found mainly in intermittent, warmer rivers, where underwater gas exchange is more problematic and risks of surfacing may be smaller. Moreover, when controlling for differences in gill density we no longer found a significant relationship between heat tolerance and its plasticity, suggesting that the previously reported positive relationship between these variables may be driven by differences in gill density. Differences in environmental conditions between the preferred habitats could simultaneously select for characteristic differences in both thermal tolerance and gill density. Such simultaneous selection may have resulted in a non-causal association between cold tolerance and gill density. For heat tolerance, the correlations with gill density could reflect a causal relationship. Species relying strongly on diffusive oxygen uptake via setal tracheal gills may have a reduced oxygen supply capacity and may be left with fewer options for matching oxygen uptake to oxygen demand during acclimation, which could explain their reduced heat tolerance and limited plasticity. Our study helps shed light on the mechanisms that underpin thermal tolerance and plasticity in diving air-breathing ectotherms, and explores how differences in thermal tolerance across species are linked to their selected habitat, morphological adaptations and evolutionary history

The impact of ocean acidification and warming on the skeletal mechanical properties of the sea urchin Paracentrotus lividus from laboratory and field observations

Increased atmospheric CO2 concentration is leading to changes in the carbonate chemistry and the temperature of the ocean. The impact of these processes on marine organisms will depend on their ability to cope with those changes, particularly the maintenance of calcium carbonate structures. Both a laboratory experiment (long-term exposure to decreased pH and increased temperature) and collections of individuals from natural environments characterized by low pH levels (individuals from intertidal pools and around a CO2 seep) were here coupled to comprehensively study the impact of near-future conditions of pH and temperature on the mechanical properties of the skeleton of the euechinoid sea urchin Paracentrotus lividus. To assess skeletal mechanical properties, we characterized the fracture force, Young's modulus, second moment of area, material nanohardness, and specific Young's modulus of sea urchin test plates. None of these parameters were significantly affected by low pH and/or increased temperature in the laboratory experiment and by low pH only in the individuals chronically exposed to lowered pH from the CO2 seeps. In tidal pools, the fracture force was higher and the Young's modulus lower in ambital plates of individuals from the rock pool characterized by the largest pH variations but also a dominance of calcifying algae, which might explain some of the variation. Thus, decreases of pH to levels expected for 2100 did not directly alter the mechanical properties of the test of P. lividus. Since the maintenance of test integrity is a question of survival for sea urchins and since weakened tests would increase the sea urchins' risk of predation, our findings indicate that the decreasing seawater pH and increasing seawater temperature expected for the end of the century should not represent an immediate threat to sea urchins vulnerability

A comparison of life-history traits in calcifying Spirorbinae polychaetes living along natural pH gradients

© Inter-Research 2018. Low-pH vent systems are ideal natural laboratories to study the consequences of long-term low-pH exposure on marine species and thus identify life-history traits associated with low-pH tolerance. This knowledge can help to inform predictions on which types of species may be less vulnerable in future ocean acidification (OA) scenarios. Accordingly, we investigated how traits of calcifying polychaete species (Serpulidae, Spirorbinae) varied with pH using a functional trait analysis at 2 natural pH gradients around the Castello Aragonese islet off Ischia, Italy. We first observed the distribution and abundance patterns of all calcifying polychaete epiphytes in the canopy of Posidonia oceanica seagrass across these gradients. We then used laboratory trials to compare fecundity, settlement success, and juvenile survival in the dominant species from a control (Pileolaria militaris Claparède, 1870) and a low-pH site (Simplaria sp.). We found significantly higher reproductive output, juvenile settlement rates, and juvenile survival in Simplaria sp. individuals from the low-pH site, compared to P. militaris individuals from control pH sites, when observed in their respective in situ pH conditions. Our results suggest that tolerance to low pH may result, in part, from traits associated with successful reproduction and rapid settlement under low-pH conditions. This finding implies that other species with similar life-history traits may respond similarly, and should be targeted for future OA tolerance research

Stage-Specific Changes in Physiological and Life-History Responses to Elevated Temperature and Pco2 during the Larval Development of the European Lobster Homarus gammarus (L.)

An organism’s physiological processes form the link between its life-history traits and the prevailing environmental conditions, especially in species with complex life cycles. Understanding how these processes respond to changing environmental conditions, thereby affecting organismal development, is critical if we are to predict the biological implications of current and future global climate change. However, much of our knowledge is derived from adults or single developmental stages. Consequently, we investigated the metabolic rate, organic content, carapace mineralization, growth, and survival across each larval stage of the European lobster Homarus gammarus, reared under current and predicted future ocean warming and acidification scenarios. Larvae exhibited stage-specific changes in the temperature sensitivity of their metabolic rate. Elevated Pco2 increased C∶N ratios and interacted with elevated temperature to affect carapace mineralization. These changes were linked to concomitant changes in survivorship and growth, from which it was concluded that bottlenecks were evident during H. gammarus larval development in stages I and IV, the transition phases between the embryonic and pelagic larval stages and between the larval and megalopa stages, respectively. We therefore suggest that natural changes in optimum temperature during ontogeny will be key to larvae survival in a future warmer ocean. The interactions of these natural changes with elevated temperature and Pco2 significantly alter physiological condition and body size of the last larval stage before the transition from a planktonic to a benthic life style. Thus, living and growing in warm, hypercapnic waters could compromise larval lobster growth, development, and recruitment. -- Keywords : Homarus gammarus ; ocean warming ; ocean acidification ; life history ; larval development ; seafood

The effects of elevated temperature and PCO2 on the energetics and haemolymph pH homeostasis of juveniles of the European lobster, Homarus gammarus

Regulation of extracellular acid–base balance, while maintaining energy metabolism, is recognised as an important aspect when defining an organism's sensitivity to environmental changes. This study investigated the haemolymph buffering capacity and energy metabolism (oxygen consumption, haemolymph [l-lactate] and [protein]) in early benthic juveniles (carapace length <40 mm) of the European lobster, Homarus gammarus, exposed to elevated temperature and PCO2. At 13°C, H. gammarus juveniles were able to fully compensate for acid–base disturbances caused by the exposure to elevated seawater PCO2 at levels associated with ocean acidification and carbon dioxide capture and storage (CCS) leakage scenarios, via haemolymph [HCO3−] regulation. However, metabolic rate remained constant and food consumption decreased under elevated PCO2, indicating reduced energy availability. Juveniles at 17°C showed no ability to actively compensate haemolymph pH, resulting in decreased haemolymph pH particularly under CCS conditions. Early benthic juvenile lobsters at 17°C were not able to increase energy intake to offset increased energy demand and therefore appear to be unable to respond to acid–base disturbances due to increased PCO2 at elevated temperature. Analysis of haemolymph metabolites suggests that, even under control conditions, juveniles were energetically limited. They exhibited high haemolymph [l-lactate], indicating recourse to anaerobic metabolism. Low haemolymph [protein] was linked to minimal non-bicarbonate buffering and reduced oxygen transport capacity. We discuss these results in the context of potential impacts of ongoing ocean change and CCS leakage scenarios on the development of juvenile H. gammarus and future lobster populations and stocks