Although there is much controversy regarding the effects of ocean acidification on the behaviour of marine fish, marine invertebrates have been much less studied. Dungeness crabs, Metacarcinus magister, are found on the West coast of North American and their commercial and recreational fishery is one of the most valuable fishery in the Pacific region, with annual revenues of $220 million. Dungeness crabs live in the deep-sea and enter intertidal areas in order to find food. Previous studies have found that they routinely encounter pCO2 concentrations of up to 1300 µatm in their coastal habitat and that these levels of ocean acidification can affect larval development and mechanoreceptors. We exposed adult Dungeness crabs to control (600 µatm) and high pCO2 (1300 µatm) for 10 days and assessed their behaviour and physiology using electrophysiology, gene expression, immunohistochemistry and transmission electron microscopy of their olfactory organs, the antennules. Dungeness crabs exposed to high pCO2 had a 25% lower rate of antennular flicking rate in response to all concentrations of cadaverine, a food cue, than crabs exposed to control pCO2. No differences in antennular flicking were found in response to ammonium chloride, a deterant, however there was a large increase in the expression of Rh proteins that function as ammonia transporters in their antennules indicating a potential compensatory mechanism. We propose that a more holistic approach to the overall question of the effects of ocean acidification needs to be taken at multiple levels of biological organization and using environmentally relevant odorants and concentrations.

The effects of simulated ocean acidification on the behaviour and physiology of the economically important Dungeness crab, Metacarcinus magister

Anthropogenic increases in atmospheric CO2 levels are raising seawater temperatures, lowering seawater oxygen concentrations and pH (‘climate-related stressors’, CRS), among other changes. Under such change, some marine groups, such as stony corals, may have less ability to tolerate stress than others, potentially leading to population loss and thereby extinction. However, whether these vulnerabilities directly scale up to extinction risk, or tend to be somehow compensated e.g. by rapid range shifts, is unclear because few modern, global extinctions are unequivocally caused by CRS. We use meta-analysis to attempt a quantitative cross-scale evaluation of the role of CRS as extinction triggers. We do this by comparing individual responses to CRS in laboratory experiments and the range shift responses to global warming over recent decades, to extinction selectivity at ancient hyperthermal events and across the sum of metazoan evolutionary history, the Phanerozoic aeon. Clades and traits with strong negative responses to experimental CRS are most likely to go extinct at hyperthermal events, their genera also having the shortest geological durations. Among CRS, the synergistic combination of seawater warming and hypoxia has the most severe impact on marine organism performance. Response details suggest chiefly metabolic constraints in setting organism performance responses to CRS, which appear to scale up to extinction probabilities of past (and potentially future?) hyperthermal events. Ecological experiments are the only way to test underlying physiological mechanisms. Meanwhile, the fossil record documents myriad extinctions, often with strong selectivity patterns, that amount to mass proportions under hyperthermal conditions. Uniting the strengths of the two approaches may enrich our abilities to predict the future.

A dangerous synergy of warming and hypoxia: the past and present for the future

Ectothermic animals represent most of the animal diversity on the planet and yet, are the most challenged by rising temperatures. As such, understanding the factors affecting thermal tolerance is crucial for predicting the impact climate change will have on ectotherms. However, the role developmental plasticity plays in allowing populations to cope with thermal extremes is poorly understood. Neglecting how early environmental experiences shape thermal tolerance (i.e., developmental plasticity) may be an important oversight given that early life experiences have major and often persistent effects on phenotypes. To quantify the acute and persistent influence of early thermal environments on thermal tolerance, we systematically reviewed 6000 studies and meta-analysed data from 150 studies. In this talk, I will address the following questions: How much do early thermal environments impact heat tolerance, and is that enough to compensate for rising temperatures? Are embryos more plastic than juveniles? Do early thermal environments have persistent influence on heat tolerance? What is the current state of knowledge and what are pressing future directions in the field?

Developmental plasticity in thermal tolerance: ontogenetic variation, persistence, and future directions

Phenotypic plasticity can increase resilience of animals to environmental change, and can therefore be important in naturally variable environments and under anthropogenic climate change. Phenotypic plasticity presents at three time scales, within-individual acclimation, developmental plasticity, and transgenerational effects. These different forms of plasticity can adjust phenotypes to at least partially buffer the organism from potentially harmful environmental conditions. Plasticity can thereby be important for population persistence and species survival. Conservation is commonly applied in a species-specific ecological context. However, it may be that populations within species have different capacities for plasticity, which may render the species as a whole more resilient to change via the portfolio effect. We tested this hypothesis by implementing novel meta-analytic approaches to quantify plastic capacities across populations of ectothermic species. We determined whether moderators including ecosystem (aquatic and terrestrial), plastic mechanisms (acclimation, developmental and transgenerational) and environmental variables (temperature and salinity) impact variability in plasticity between populations. The outcome of this study are important for conservation and in an evolutionary context to understand the complexity of transient responses to environmental change within species.

Are there differences in plasticity between populations within species?

While hypoxia (i.e. low dissolved oxygen level in water) events occur naturally, global change and human activities have exacerbated their strength and temporal fluctuations. As populations may not be able to escape the hypoxic conditions, especially in freshwater ponds, it is crucial to understand how organisms can adjust and adapt to these fluctuating environments. When directly exposed, individuals may be able to adjust their phenotypes through plasticity, but continued exposure to hypoxia over generations may require adaptation and evolution. As the mitochondrial metabolism is the key component that fuel aerobic functions, the individual capacity to respond to the environmental change in oxygen availability is likely to rely on mitochondrial functions. Using two populations of wild three-spined sticklebacks (Gasterosteus aculeatus) exposed to different levels of hypoxia conditions in their natural habitats and experimentally exposed to fluctuating hypoxia (20% air saturation during the night and 100% during the day), we investigated the fish metabolic plastic and evolutionary response.  We showed adaptation in fish growth and metabolic rate, fish exposed to hypoxia in their natural habitats possessing higher metabolic capacity, but limited evidence for plasticity to the experimental conditions. These responses were supported by the muscle mitochondrial metabolism, for which similar adaptation were observed. However, no differences were observed in the brain mitochondrial metabolism, suggesting tissue specific response to environmental changes. Overall, these results highlight the capacity of fish to adapt environmental changes across generations, relying on mitochondrial adaptation.

Fish metabolic response to freshwater hypoxia: plasticity and adaptation

Monocotyledons comprise about one-quarter of all flowering plants, colonize all bio-geographical and climatic regions of the planet and reveal a striking growth form diversity ranging from tiny swimming to large arborescent species. This growth form diversity is based on a rigid fibrous vascular network embedded into a viscoelastic parenchyma matrix and is established and limited by primary vascular growth. Only few monocot genera, all belonging to the Asparagales, are able to modify their tissue structure via secondary thickening growth. Despite the limitations on tissue level, monocots evolved diverse mechanical properties, that are based on their fiber reinforced bauplan such as very stiff bamboo culms or highly compliant pulvini. However, the mechanical architecture of monocots, and here especially the nodus, remain relatively unexplored, despite the fact that it is the crucial connecting element between internodes and laterals. Here I present how biomechanical experiments and 3D imaging using µCT and MRI techniques as well as plant specific image optimization techniques help to unravel structural design patterns in monocots. 

Structural diversity and biomechanics in monocots

Among-species comparisons have been a mainstay of comparative, ecological, and evolutionary physiology for many decades. The ongoing collation of trait databases coupled with the widespread adoption of phylogenetic comparative methods has created fertile ground for the demonstration of new patterns, and for the re-examination of well-known patterns. However, the increases in data richness and analytical sophistication have not changed the fundamental limitations of correlational approaches. Here I explore these limitations, focussing on the important differences between congruence, correlation, and causation. I then use multivariate phylogenetic mixed models to demonstrate the limited extent to which among-species patterns can be used to infer the within-species processes that generate them.

What meta-analyses and comparative analyses can, and can't, tell us about biological phenomena

Giant clams are threatened by overexploitation for human consumption, their valuable shells and the aquarium trade. Consequently, these iconic megafauna are extinct in some former areas of their range and included in the IUCN Red List of Threatened Species and CITES list. Now, giant clams are also threatened by rapid environmental change from both a suite of local- to regional-scale stressors, such poor water quality and pollution, and global change stressors, including ocean heating and acidification. The interplay between local- to regional-scale and global-scale drivers is likely to cause an array of lethal and sub-lethal effects, potentially limiting giant clam depth distribution on coral reefs and decreasing suitable habitat area within natural ranges. International efforts urgently need to reduce CO2 emissions to avoid lethal and sub-lethal effects on giant clams. Meanwhile, knowledge of ecological and physiological responses to local–regional and global stressors could play a critical role in the conservation of these species through rapid environmental change. Further work on how biological responses translate into habitat requirements as global change progresses, selective breeding for resilience, the capacity for rapid adaptive responses of the giant clam holobiont, and valuing tourism potential may help improve the prospects of these charismatic megafauna over coming decades.

Conserving threatened coastal wildlife during rapid environmental change: using biological responses to inform management strategies of giant clams

The ability of populations to expand their geographic ranges, whether as invaders or climate migrants, presents among the most serious global problems today. However, fundamental mechanisms that enable certain populations to rapidly adapt to novel habitats remain poorly understood. In recent years, populations of the copepod Eurytemora affinis species complex have invaded freshwater habitats multiple times independently from saline sources. These copepods are dominant grazers in aquatic habitats throughout the Northern Hemisphere and support major fisheries. Intriguingly, evolutionary changes during these salinity transitions often involved the same loci, with selection often acting on the same SNPs (alleles), in wild populations and laboratory selection lines. In our laboratory natural selection experiment, the same SNPs were favored across replicate selection lines far beyond expectations. In both wild populations and laboratory selection lines, ion transporter genes appeared as the dominant functional category under selection. Using extensive simulations, we found that this degree of parallelism was consistent with synergistic epistasis among alleles responding in concert across replicate selection lines for this polygenic trait (salinity tolerance). The effect of synergistic epistasis appeared greater than selection from balanced polymorphisms in promoting parallel evolution. Our results were consistent with mechanisms of ion uptake from dilute habitats, requiring the coordinated action of cooperating ion transporter proteins. Most notably, our results suggest that a very specific set of ion transporter alleles might be necessary for freshwater adaptation to occur in this system, pointing to a canalized evolutionary pathway. Thus, we find strong support for a novel and potentially widespread mechanism, namely positive epistasis, in promoting this parallel and canalized response. This research is funded by NSF-OCE, NSF-DEB, and ANR (Macron’s Make Our Planet Great Again award).

Mechanisms of parallel adaptation in a widespread copepod

Climate change is increasing both the average ambient temperature and the frequency and severity of heat waves. While direct mortality induced by heat waves is increasingly reported, sub-lethal effects are also likely to impact population dynamics and persistence. We hypothesized that accelerated cellular ageing could be a cost of being exposed to higher ambient temperature. We tested this hypothesis in two common European passerine species by experimentally increasing nest box temperature by ca. 2°C during postnatal growth and measuring telomere length as a biomarker of ageing. In great tits, we also estimated the impact on medium-term survival and measured a large set of physiological markers including thyroid hormones, glucocorticoid signaling, oxidative stress, mitochondrial density and telomere maintenance mechanisms. We show that in both species, increasing early-life temperature does not affect growth or survival to fledging, but leads to an acceleration in the shortening of telomeres. In great tits, such shortening of telomeres was not explained by increased oxidative stress levels, but more likely by an increase in energy demand (i.e. higher thyroid hormones levels, increased expression of glucocorticoid receptor, increased mitochondrial density) leading to a reduction in telomere maintenance mechanisms (i.e. decrease in the gene expression of telomerase and protective shelterin). Additionally, medium-term survival was reduced from 34% in control nests to 19% in heated nests. Our results thus suggest that climate warming might affect cellular ageing in wild passerine populations, with potential impact on population dynamics and persistence.

From climate warming to accelerated cellular ageing: insights from two experimental studies in wild passerine birds

Despite ~80% of all animal species undergoing metamorphosis, the effect of this dramatic developmental process on telomere dynamics is unknown. Given that the rate of telomere shortening has been shown in non-metamorphosing species to be influenced by environmental harshness, the question arises as to whether the re-modelling of tissues that occurs during metamorphosis allows an individual to re-set its telomeres and so leave behind this legacy of past environments. This issue is pertinent to amphibians, a group likely to be heavily impacted in the larval stage (i.e., before metamorphosis) by environmental events such as global warming. We will first briefly discuss the current knowledge gaps in the study of amphibian telomeres, then present new data on telomere length across different tissues and developmental stages (from larva to adulthood) in the frog Xenopus laevis. We will also examine the impact of warming conditions before and after metamorphosis on amphibian telomeres and telomerase. Our results show that telomere length is affected not only by the rate of somatic growth, but also by the degree of metamorphic transformation experienced by particular tissues: during metamorphosis, telomere length can either decline, remain stable or dramatically increase. Furthermore, this life history transition seems to be able to buffer the impact on telomeres of harsh conditions in early life. This leads us to suggest directions for future research on telomere dynamics in amphibians and other species with complex-life cycles.

Across the great divide: telomere dynamics through metamorphosis in amphibians

Understanding how and why metabolic rate scales allometrically with body mass in fish is of particular interest given the observed decline in the maximum body size of aquatic ectotherms under climate warming. Size-dependent oxygen limitation has been proposed to drive these body size declines, particularly at warmer temperatures. If this is true, then in warm settings and with an excess oxygen supply (hyperoxia) we would expect scaling exponents to steepen as larger fish would require comparatively more oxygen to fulfill their proposed debt. To test this, we measured the aerobic metabolic performance of Galaxias maculatus upon acute exposure to hyperoxia (150% air saturation) and following five months of acclimation to hyperoxia, at 15°C and 20°C. Despite hyperoxia acclimation, scaling exponents for standard and maximum metabolic rates did not differ from normoxia-acclimated conspecifics, implying that oxygen limitation does not regulate allometric scaling. Interestingly, the scaling exponents for standard metabolic rate in normoxia- and hyperoxia-acclimated fish at 15°C were particularly high (1.05 and 1.08, respectively). Further investigation revealed that these high exponents were likely driven by differences in the reproductive state of smaller (immature) vs. larger (mature) fish, illustrating the increased energetic demands of the reproductive process and the need to account for reproductive stage when assessing metabolic scaling in fish.

Underline digital video library

The effects of simulated ocean acidification on the behaviour and physiology of the economically important Dungeness crab, Metacarcinus magister

A dangerous synergy of warming and hypoxia: the past and present for the future

Developmental plasticity in thermal tolerance: ontogenetic variation, persistence, and future directions

Are there differences in plasticity between populations within species?

Fish metabolic response to freshwater hypoxia: plasticity and adaptation

Structural diversity and biomechanics in monocots

What meta-analyses and comparative analyses can, and can't, tell us about biological phenomena

Conserving threatened coastal wildlife during rapid environmental change: using biological responses to inform management strategies of giant clams

Mechanisms of parallel adaptation in a widespread copepod

From climate warming to accelerated cellular ageing: insights from two experimental studies in wild passerine birds

Across the great divide: telomere dynamics through metamorphosis in amphibians

Effects of hyperoxia and reproductive state on the metabolic scaling of a temperate fish Galaxias maculatus

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