Morgan W. Kelly

Temperature and CO 2 additively regulate physiology, morphology and genomic responses of larval sea urchins, Strongylocentrotus purpuratus

Ocean warming and ocean acidification, both consequences of anthropogenic production of CO2, will combine to influence the physiological performance of many species in the marine environment. In this study, we used an integrative approach to forecast the impact of future ocean conditions on larval purple sea urchins (Strongylocentrotus purpuratus) from the northeast Pacific Ocean. In laboratory experiments that simulated ocean warming and ocean acidification, we examined larval development, skeletal growth, metabolism and patterns of gene expression using an orthogonal comparison of two temperature (13°C and 18°C) and pCO2 (400 and 1100 μatm) conditions. Simultaneous exposure to increased temperature and pCO2 significantly reduced larval metabolism and triggered a widespread downregulation of histone encoding genes. pCO2 but not temperature impaired skeletal growth and reduced the expression of a major spicule matrix protein, suggesting that skeletal growth will not be further inhibited by ocean warming. Importantly, shifts in skeletal growth were not associated with developmental delay. Collectively, our results indicate that global change variables will have additive effects that exceed thresholds for optimized physiological performance in this keystone marine species.

Trade-Offs, Geography, and Limits to Thermal Adaptation in a Tide Pool Copepod

Antagonistic correlations among traits may slow the rate of adaptation to a changing environment. The tide pool copepod Tigriopus californicus is locally adapted to temperature, but within populations, the response to selection for increased heat tolerance plateaus rapidly, suggesting either limited variation within populations or costs of increased tolerance. To measure possible costs of thermal tolerance, we selected for increased upper lethal limits for 10 generations in 22 lines of T. californicus from six populations. Then, for each line, we measured six fitness-related traits. Selected lines showed an overall increase in male and female body sizes, fecundity, and starvation resistance, suggesting a small benefit from (rather than costs of) increased tolerance. The effect of selection on correlated traits also varied significantly by population for five traits, indicating that the genetic basis for the selection response differed among populations. Our results suggest that adaptation was limited by the presence of variation within isolated populations rather than by costs of increased tolerance.

Mechanistic species distribution modelling as a link between physiology and conservation

Species distribution modeling is the most common method of estimating climate change impacts on biodiversity. In this review, we argue a need for collaboration among physiologists, modelers and conservationists to parameterize models with physiological information in order to increase their accuracy and advance the field of conservation physiology.

Trait Correlations in the Genomics Era

Thinking about the evolutionary causes and consequences of trait correlations has been dominated by quantitative genetics theory that is focused on hypothetical loci. Since this theory was initially developed, technology has enabled the identification of specific genetic variants that contribute to trait correlations. Here, we review studies of the genetic basis of trait correlations to ask: What has this new information taught us? We find that causal variants can be pleiotropic and/or linked in different ways, indicating that pleiotropy and linkage are not alternative genetic mechanisms. Further, many trait correlations have a polygenic basis, suggesting that both pleiotropy and linkage likely contribute. We discuss implications of these findings for the evolutionary causes and consequences of trait correlations.

Physiological plasticity and local adaptation to elevated pCO2 in calcareous algae: An ontogenetic and geographic approach

To project how ocean acidification will impact biological communities in the future, it is critical to understand the potential for local adaptation and the physiological plasticity of marine organisms throughout their entire life cycle, as some stages may be more vulnerable than others. Coralline algae are ecosystem engineers that play significant functional roles in oceans worldwide and are considered vulnerable to ocean acidification. Using different stages of coralline algae, we tested the hypothesis that populations living in environments with higher environmental variability and exposed to higher levels of pCO2 would be less affected by high pCO2 than populations from a more stable environment experiencing lower levels of pCO2. Our results show that spores are less sensitive to elevated pCO2 than adults. Spore growth and mortality were not affected by pCO2 level; however, elevated pCO2 negatively impacted the physiology and growth rates of adults, with stronger effects in populations that experienced both lower levels of pCO2 and lower variability in carbonate chemistry, suggesting local adaptation. Differences in physiological plasticity and the potential for adaptation could have important implications for the ecological and evolutionary responses of coralline algae to future environmental changes.

Adaptation to climate change: trade-offs among responses to multiple stressors in an intertidal crustacean

Trade‐offs may influence both physiological and evolutionary responses to co‐occurring stressors, but their effects on both plastic and adaptive responses to climate change are poorly understood. To test for genetic and physiological trade‐offs incurred in tolerating multiple stressors, we hybridized two populations of the intertidal copepod Tigriopus californicus that were divergent for both heat and salinity tolerance. Starting in the F2 generation, we selected for increased tolerance of heat, low salinity, and high salinity in replicate lines. After five generations of selection, heat‐selected lines had greater heat tolerance but lower fecundity, indicating an energetic cost to tolerance. Lines selected for increased salinity tolerance did not show evidence of adaptation to their respective environments; however, hypo‐osmotic selection lines showed substantial loss of tolerance to hyperosmotic stress. Neither of the salinity selection regimes resulted in diminished heat tolerance at ambient salinity; however, simultaneous exposure to heat and hypo‐osmotic stress led to decreased heat tolerance, implying a physiological trade‐off in tolerance to the two stressors. When we quantified the transcriptomic response to heat and salinity stress via RNA sequencing, we observed little overlap in the stress responses, suggesting the observed synergistic effects of heat and salinity stress were driven by competing energetic demands, rather than shared stress response pathways.

Adaptation to heat stress reduces phenotypic and transcriptional plasticity in a marine copepod

Summary 1.Organisms may respond to changing environments through phenotypic plasticity or adaptive evolution. These two processes are not mutually exclusive, and may either dampen or strengthen each others effects, depending on the genetic correlation between trait values and the slopes of their norms of reaction. 2.To examine the effect of adaptation to heat stress on the plasticity of heat tolerance we hybridized populations of the crustacean Tigriopus californicus that show divergent phenotypes for heat tolerance. We then selected for increased heat tolerance in hybrids and measured heat tolerance and the phenotypic plasticity of heat tolerance in both selected lines and unselected controls. 3.To test whether changes in phenotypic plasticity were associated with changes in the plasticity of gene expression, we also sequenced transcriptomes of selected and unselected lines, both under heat shock and at ambient temperatures. 4.We observed increased heat tolerance in selected lines, but also lower phenotypic and transcriptional plasticity in response to heat stress. The plastic response to heat stress was highly enriched for hydrolytic and catalytic activities, suggesting a prominent role for degradation of mis-folded proteins. 5.Our findings have important implications for biological responses to climate change: if adaptation to environmental stress reduces plasticity, then plasticity and adaptive evolution will make overlapping, rather than additive contributions to buffering populations from environmental change. This article is protected by copyright. All rights reserved.

Transcriptomics reveal transgenerational effects in purple sea urchin embryos: Adult acclimation to upwelling conditions alters the response of their progeny to differential pCO2 levels

Understanding the mechanisms with which organisms can respond to a rapidly changing ocean is an important research priority in marine sciences, especially in the light of recent predictions regarding the pace of ocean change in the coming decades. Transgenerational effects, in which the experience of the parental generation can shape the phenotype of their offspring, may serve as such a mechanism. In this study, adult purple sea urchins, Strongylocentrotus purpuratus, were conditioned to regionally and ecologically relevant pCO2 levels and temperatures representative of upwelling (colder temperature and high pCO2) and nonupwelling (average temperature and low pCO2) conditions typical of coastal upwelling regions in the California Current System. Following 4.5 months of conditioning, adults were spawned and offspring were raised under either high or low pCO2 levels, to examine the role of maternal effects. Using RNA‐seq and comparative transcriptomics, our results indicate that differential conditioning of the adults had an effect on the gene expression patterns of the progeny during the gastrula stage of early development. For example, maternal conditioning under upwelling conditions intensified the transcriptomic response of the progeny when they were raised under high versus low pCO2 conditions. Additionally, mothers that experienced upwelling conditions produced larger progeny. The overall findings of this study are complex, but do suggest that transgenerational plasticity in situ could act as an important mechanism by which populations might keep pace with rapid environmental change.

Phenotypic and transcriptomic responses to salinity stress across genetically and geographically divergent Tigriopus californicus populations

Species inhabiting the North American west coast intertidal must tolerate an extremely variable environment, with large fluctuations in both temperature and salinity. Uncovering the mechanisms for this tolerance is key to understanding species’ persistence. We tested for differences in salinity tolerance between populations of Tigriopus californicus copepods from locations in northern (Bodega Reserve) and southern (San Diego) California known to differ in temperature, precipitation and humidity. We also tested for differences between populations in their transcriptomic responses to salinity. Although these two populations have ~20% mtDNA sequence divergence and differ strongly in other phenotypic traits, we observed similarities in their phenotypic and transcriptomic responses to low and high salinity stress. Salinity significantly affected respiration rate (increased under low salinity and reduced under high salinity), but we found no significant effect of population on respiration or a population by salinity interaction. Under high salinity, there was no population difference in knock‐down response, but northern copepods had a smaller knock‐down under low salinity stress, corroborating previous results for T. californicus. Northern and southern populations had a similar transcriptomic response to salinity based on a principle components analysis, although differential gene expression under high salinity stress was three times lower in the northern population compared to the southern population. Transcripts differentially regulated under salinity stress were enriched for “amino acid transport” and “ion transport” annotation categories, supporting previous work demonstrating that the accumulation of free amino acids is important for osmotic regulation in T. californicus.

Host and Symbionts in Pocillopora damicornis Larvae Display Different Transcriptomic Responses to Ocean Acidification and Warming

As global ocean change progresses, reef-building corals and their early life history stages will rely on physiological plasticity to tolerate new environmental conditions. Larvae from brooding coral species contain algal symbionts upon release, which assist with the energy requirements of dispersal and metamorphosis. Global ocean change threatens the success of larval dispersal and settlement by challenging the performance of the larvae and of the symbiosis. In this study, larvae of the reef-building coral Pocillopora damicornis were exposed to elevated pCO2 and temperature to examine the performance of the coral and its symbionts in situ and better understand the mechanisms of physiological plasticity and stress tolerance in response to multiple stressors. We generated a de novo holobiont transcriptome containing coral host and algal symbiont transcripts and bioinformatically filtered the assembly into host and symbiont components for downstream analyses. Seventeen coral genes were differentially expressed in response to the combined effects of pCO2 and temperature. In the symbiont, 89 genes were differentially expressed in response to pCO2. Our results indicate that many of the whole-organism (holobiont) responses previously observed for P. damicornis larvae in scenarios of ocean acidification and warming may reflect the physiological capacity of larvae to cope with the environmental changes without expressing additional protective mechanisms. At the holobiont level, the results suggest that the responses of symbionts to future ocean conditions could play a large role in shaping success of coral larval stages.