Rising ocean temperatures and extreme temperature events have precipitated declines and local extinctions in many marine species globally, but patterns of loss are often uneven across species ranges for reasons that are poorly understood.Knowledge of the extent of local adaptation and gene flow may explain such patterns and help predict future trajectories under scenarios of climate change. We test the extent to which local differentiation in thermal tolerance is influenced by gene flow and local adaptation using a widely distributed intertidal seaweed (Hormosira banksii) from temperate Australia. Population surveys across ~2,000 km of the species range revealed strong genetic structuring at regional and local scales (global F ST = 0.243) reflecting extremely limited gene flow, while common garden experiments (14-day exposures to 15, 18, 21°C) revealed strong site differences in early development and mortality in response to elevated temperature. Embryos from many sites spanning a longitudinal thermal gradient showed suppressed development and increased mortality to elevated water temperatures, but populations originating from warmer and more variable thermal environments tended to be less susceptible to warming. Notably, there was significant local-scale variation in the thermal responses of embryos within regions which was corroborated by the finding of small-scale genetic differences. We expect the observed genetic and phenotypic differentiation to lead to uneven responses to warming sea surface temperatures in this important marine foundation species. The study highlights the challenges of predicting species responses to thermal stress and the importance of management strategies that incorporate evolutionary potential for "climate-proofing" marine ecosystems.

Understanding responses of marine algae to changing ocean temperatures requires knowledge of the impacts of elevated temperatures and the likelihood of adaptation to thermal stress. The potential for rapid evolution of thermal tolerance is dependent on the levels of heritable genetic variation in response to thermal stress within a population. Here, we use a quantitative genetic breeding design to establish whether there is a heritable variation in thermal sensitivity in two populations of a habitat-forming intertidal macroalga, Hormosira banksii (Turner) Descaisne. Gametes from multiple parents were mixed and growth and photosynthetic performance were measured in the resulting embryos, which were incubated under control and elevated temperature (20°C and 28°C). Embryo growth was reduced at 28°C, but significant interactions between male genotype and temperature in one population indicated the presence of genetic variation in thermal sensitivity. Selection for more tolerant genotypes thus has the ability to result in the evolution of increased thermal tolerance. Furthermore, genetic correlations between embryos grown in the two temperatures were positive, indicating that those genotypes that performed well in elevated temperature also performed well in control temperature. Chlorophyll a fluorescence measurements showed a marked decrease in maximum quantum yield of photosystem II (PSII) under elevated temperature. There was an increase in the proportion of energy directed to photoinhibition (nonregulated nonphotochemical quenching) and a concomitant decrease in energy used to drive photochemistry and xanthophyll cycling (regulated nonphotochemical quenching). However, PSII performance between genotypes was similar, suggesting that thermal sensitivity is related to processes other than photosynthesis.

Temperate intertidal shores globally are often dominated by habitat-forming seaweeds, but our knowledge of these systems is heavily biased towards northern hemisphere species. Rocky intertidal shores throughout Australia and New Zealand are dominated by a single monotypic species, Hormosira banksii. This species plays a key role in facilitating biodiversity on both rocky shores and estuarine habitats, yet we know little about the processes that structure populations. Herein we characterise the genetic diversity and structure of Hormosira and demonstrate strong restrictions to gene flow over small spatial scales, as well as between estuarine and open coast populations. Estuarine ecotypes were often genetically unique from nearby open coast populations, possibly due to extant reduced gene flow between habitats, founder effects and coastal geomorphology. Deviations from random mating in many locations suggest complex demographic processes are at play within shores, including clonality in estuarine populations. Strong isolation by distance in Hormosira suggests that spatial management of intertidal habitats will necessitate a network of broad-scale protection. Understanding patterns of genetic diversity and gene flow in this important ecosystem engineer will enhance the ability to manage, conserve and restore this key species into the future.

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Experimentation at sea provides insight into which traits of ocean microbes are linked to performance in situ. Here we show distinct patterns in thermal tolerance of microbial phototrophs from adjacent water masses sampled in the southwest Pacific Ocean, determined using a fluorescent marker for reactive oxygen species (ROS). ROS content of pico-eukaryotes was assessed after 1, 5 and 25 h of incubation along a temperature gradient (15.6-32.1°C). Pico-eukaryotes from the East Australian Current (EAC) had relatively constant ROS and showed greatest mortality after 25 h at 7°C below ambient, whereas those from the Tasman Sea had elevated ROS in both warm and cool temperature extremes and greatest mortality at temperatures 6-10°C above ambient, interpreted as the outcome of thermal stress. Tracking of water masses within an oceanographic circulation model showed populations had distinct thermal histories, with EAC pico-eukaryotes experiencing higher average temperatures for at least 1 week prior to sampling. While acclimatization and community assembly could both influence biological responses, this study clearly demonstrates that phenotypic divergence occurs along planktonic drift trajectories.

Species inhabiting warm-edge populations of their distribution are suggested to be at the forefront of global warming due to reduced fitness, limited gene flow and living close to their physiological thermal limits. Determining the scale that governs thermal niche and the functional responses of habitat-forming species to environmental stressors is critical for successful conservation efforts, particularly as coastal ecosystems are impacted by global change. Here, we examine the susceptibility of warm-edge populations to warming, in the habitat-forming macroalga, Hormosira banksii, from southeastern Australia. We use a quantitative breeding design to quantify intraspecific variation in thermal performance (growth, ontogenic development and photosynthetic efficiency) of different genotypes sourced from sites at the equatorward distributional edge (warm-edge) and those toward the center of its distribution (non-edge). The genetic diversity and structure of H. banksii was also examined using microsatellite markers amongst the same sites. Our results found variable responses in thermal performance for growth and development. Warm-edge germlings grew optimally in lower temperatures tested and had narrower thermal breadth compared to non-edge germlings which grew in higher and more broader temperatures. Warm-edge germlings however, showed greater plasticity to tolerate high light indicated by a greater proportion of energy being dissipated as regulated non-photochemical quenching [Y(NPQ)] than non-regulated non-photochemical quenching [Y(NO)]. Overall genetic diversity was lower at the warm-edge location with evidence of increased structuring and reduced gene flow in comparison to the non-edge location. Evidence of genetic structuring was not found locally between high and low shore within sites. Together, these data suggest that non-edge populations may be "thermally buffered" from increased temperatures associated with ocean warming. Warm-edge populations of H. banksii, however, may be vulnerable to warming, due to narrower thermal breadth and sensitivity to higher temperatures, with genetic impoverishment through loss of individuals likely to further reduce population viability.

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