Transcriptomic responses in the nervous system and correlated behavioural changes of a cephalopod exposed to ocean acidification.

BACKGROUND: The nervous system is central to coordinating behavioural responses to environmental change, likely including ocean acidification (OA). However, a clear understanding of neurobiological responses to OA is lacking, especially for marine invertebrates. RESULTS: We evaluated the transcriptomic response of the central nervous system (CNS) and eyes of the two-toned pygmy squid (Idiosepius pygmaeus) to OA conditions, using a de novo transcriptome assembly created with long read PacBio ISO-sequencing data. We then correlated patterns of gene expression with CO2 treatment levels and OA-affected behaviours in the same individuals. OA induced transcriptomic responses within the nervous system related to various different types of neurotransmission, neuroplasticity, immune function and oxidative stress. These molecular changes may contribute to OA-induced behavioural changes, as suggested by correlations among gene expression profiles, CO2 treatment and OA-affected behaviours. CONCLUSIONS: This study provides the first molecular insights into the neurobiological effects of OA on a cephalopod and correlates molecular changes with whole animal behavioural responses, helping to bridge the gaps in our knowledge between environmental change and animal responses.

Out of shape: Ocean acidification simplifies coral reef architecture and reshuffles fish assemblages.

Climate change stressors are progressively simplifying biogenic habitats in the terrestrial and marine realms, and consequently altering the structure of associated species communities. Here, we used a volcanic CO2 seep in Papua New Guinea to test in situ if altered reef architecture due to ocean acidification reshuffles associated fish assemblages. We observed replacement of branching corals by massive corals at the seep, with simplified coral architectural complexity driving abundance declines between 60% and 86% for an assemblage of damselfishes associated with branching corals. An experimental test of habitat preference for a focal species indicated that acidification does not directly affect habitat selection behaviour, with changes in habitat structural complexity consequently appearing to be the stronger driver of assemblage reshuffling. Habitat health affected anti-predator behaviour, with P. moluccensis becoming less bold on dead branching corals relative to live branching corals, irrespective of ocean acidification. We conclude that coral reef fish assemblages are likely to be more sensitive to changes in habitat structure induced by increasing pCO2 than any direct effects on behaviour, indicating that changes in coral architecture and live cover may act as important mediators of reef fish community structures in a future ocean.

Long non-coding RNAs mediate fish gene expression in response to ocean acidification.

The majority of the transcribed genome does not have coding potential but these non-coding transcripts play crucial roles in transcriptional and post-transcriptional regulation of protein-coding genes. Regulation of gene expression is important in shaping an organism's response to environmental changes, ultimately impacting their survival and persistence as population or species face global change. However, the roles of long non-coding RNAs (lncRNAs), when confronted with environmental changes, remain largely unclear. To explore the potential role of lncRNAs in fish exposed to ocean acidification (OA), we analyzed publicly available brain RNA-seq data from a coral reef fish Acanthochromis polyacanthus. We annotated the lncRNAs in its genome and examined the expression changes of intergenic lncRNAs (lincRNAs) between A. polyacanthus samples from a natural CO2 seep and a nearby control site. We identified 4728 lncRNAs, including 3272 lincRNAs in this species. Remarkably, 93.03% of these lincRNAs were species-specific. Among the 125 highly expressed lincRNAs and 403 differentially expressed lincRNAs in response to elevated CO2, we observed that lincRNAs were either neighboring or potentially trans-regulating differentially expressed coding genes associated with pH regulation, neural signal transduction, and ion transport, which are known to be important in the response to OA in fish. In summary, lncRNAs may facilitate fish acclimation and mediate the responses of fish to OA by modulating the expression of crucial coding genes, which offers insight into the regulatory mechanisms underlying fish responses to environmental changes.

How Oratosquilla oratoria compound eye response to the polarization of light: In the perspective of vision genes and related proteins.

The special rhabdom structure of the mid-band ommatidium in compound eye contributes to the mantis shrimp being the only animal species known to science that can recognize circularly polarized light (CPL). Although the number of mid-band ommatidium of Oratosquilla oratoria is reduced, the mid-band ommatidium still has orthogonal geometric interleaved rhabdom and short oval distal rhabdom, which may mean that the O. oratoria has weakened circular polarized light vision (CPLV). Here we explored the molecular mechanisms of how O. oratoria response to the polarization of light. Based on the specific expression patterns of vision-related functional genes and proteins, we suggest that the order of light response by O. oratoria compound eye was first natural light, then left-circularly polarized light (LCPL), linearly polarized light, right-circularly polarized light (RCPL) and dark. Meanwhile, we found that the expression levels of vision-related functional genes and proteins in O. oratoria compound eye under RCPL were not significantly different from those in DL, which may imply that O. oratoria cannot respond to RCPL. Furthermore, the response of LCPL is likely facilitated by the differential expression of opsin and microvilli - related functional genes and proteins (arrestin and sodium-coupled neutral amino acid transporter). In conclusion, this study systematically illustrated for the first time how O. oratoria compound eye response to the polarization of light at the genetic level, and it can improve the visual ecological theory behind polarized light vision evolution.

Warming affects routine swimming activity and novel odour response in larval zebrafish.

Temperature is a primary factor affecting the physiology of ectothermic animals and global warming of water bodies may therefore impact aquatic life. Understanding the effects of near-future predicted temperature changes on the behaviour and underlying molecular mechanisms of aquatic animals is of particular importance, since behaviour mediates survival. In this study, we investigate the effects of developmental temperature on locomotory behaviour and olfactory learning in the zebrafish, Danio rerio. We exposed zebrafish from embryonic stage to either control (28 °C) or elevated temperature (30 °C) for seven days. Overall, warming reduced routine swimming activity and caused upregulation of metabolism and neuron development genes. When exposed to olfactory cues, namely catfish cue, a non-alarming but novel odour, and conspecifics alarming cue, warming differently affected the larvae response to the two cues. An increase in locomotory activity and a large transcriptional reprogramming was observed at elevated temperature in response to novel odour, with upregulation of cell signalling, neuron development and neuron functioning genes. As this response was coupled with the downregulation of genes involved in protein translation and ATP metabolism, novel odour recognition in future-predicted thermal conditions would require energetic trade-offs between expensive baseline processes and responsive functions. To evaluate their learning abilities at both temperatures, larvae were conditioned with a mixture of conspecifics alarm cue and catfish cue. Regardless of temperature, no behavioural nor gene expression changes were detected, reinforcing our findings that warming mainly affects zebrafish molecular response to novel odours. Overall, our results show that future thermal conditions will likely impact developing stages, causing trade-offs following novel olfactory detection in the environment.

Gene losses, parallel evolution and heightened expression confer adaptations to dedicated cleaning behaviour.

BACKGROUND: Cleaning symbioses are captivating interspecific interactions in which a cleaner fish removes ectoparasites from its client, contributing to the health and diversity of natural fish communities and aquaculture systems. However, the genetic signatures underlying this specialized behaviour remain poorly explored. To shed light on this, we generated a high-quality chromosome-scale genome of the bluestreak cleaner wrasse Labroides dimidiatus, a dedicated cleaner with cleaning as primary feeding mechanism throughout its life. RESULTS: Compared with facultative and non-cleaner wrasses, L. dimidiatus was found with notable contractions in olfactory receptors implying their limited importance in dedicated cleaning. Instead, given its distinct tactile pre-conflict strategies, L. dimidiatus may rely more heavily on touch sensory perception, with heightened gene expression in the brain in anticipation of cleaning. Additionally, a reduction in NLR family CARD domain-containing protein 3 might enhance innate immunity of L. dimidiatus, probably assisting to reduce the impacts from parasite infections. In addition, convergent substitutions for a taste receptor and bone development genes across cleaners (L. dimidiatus and facultative cleaners) may provide them with evolved food discrimination abilities and jaw morphology that differentiate them from non-cleaners. Moreover, L. dimidiatus may exhibit specialized neural signal transductions for cleaning, as evidenced by positive selection in genes related to the glutamatergic synapse pathway. Interestingly, numerous glutamate receptors also demonstrated significantly higher expression in L. dimidiatus not engaged in cleaning, as compared to those involved in cleaning. Besides, apparent contractions in L. dimidiatus for protocadherins, which are responsible for neuronal development, may further promote specialized neural signal transductions in this species. CONCLUSIONS: This study reveals that L. dimidiatus harbours substantial losses in specific gene families, convergent evolutions across cleaners and a large-scale high gene expression in preparation for cleaning, allowing for adaptation to the dedicated cleaning behaviour.

Brain transcriptome of gobies inhabiting natural CO2 seeps reveal acclimation strategies to long-term acidification.

Ocean acidification (OA) is known to affect the physiology, survival, behaviour and fitness of various fish species with repercussions at the population, community and ecosystem levels. Some fish species, however, seem to acclimate rapidly to OA conditions and even thrive in acidified environments. The molecular mechanisms that enable species to successfully inhabit high CO2 environments have not been fully elucidated especially in wild fish populations. Here, we used the natural CO2 seep in Vulcano Island, Italy to study the effects of elevated CO2 exposure on the brain transcriptome of the anemone goby, a species with high population density in the CO2 seep and investigate their potential for acclimation. Compared to fish from environments with ambient CO2, gobies living in the CO2 seep showed differences in the expression of transcripts involved in ion transport and pH homeostasis, cellular stress, immune response, circadian rhythm and metabolism. We also found evidence of potential adaptive mechanisms to restore the functioning of GABAergic pathways, whose activity can be affected by exposure to elevated CO2 levels. Our findings indicate that gobies living in the CO2 seep may be capable of mitigating CO2-induced oxidative stress and maintaining physiological pH while meeting the consequent increased energetic costs. The conspicuous difference in the expression of core circadian rhythm transcripts could provide an adaptive advantage by increasing the flexibility of physiological processes in elevated CO2 conditions thereby facilitating acclimation. Our results show potential molecular processes of acclimation to elevated CO2 in gobies enabling them to thrive in the acidified waters of Vulcano Island.

Rapid evolution fuels transcriptional plasticity to ocean acidification.

Ocean acidification (OA) is postulated to affect the physiology, behavior, and life-history of marine species, but potential for acclimation or adaptation to elevated pCO2 in wild populations remains largely untested. We measured brain transcriptomes of six coral reef fish species at a natural volcanic CO2  seep and an adjacent control reef in Papua New Guinea. We show that elevated pCO2 induced common molecular responses related to circadian rhythm and immune system but different magnitudes of molecular response across the six species. Notably, elevated transcriptional plasticity was associated with core circadian genes affecting the regulation of intracellular pH and neural activity in Acanthochromis polyacanthus. Gene expression patterns were reversible in this species as evidenced upon reduction of CO2 following a natural storm-event. Compared with other species, Ac. polyacanthus has a more rapid evolutionary rate and more positively selected genes in key functions under the influence of elevated CO2 , thus fueling increased transcriptional plasticity. Our study reveals the basis to variable gene expression changes across species, with some species possessing evolved molecular toolkits to cope with future OA.

The alternative splicing landscape of a coral reef fish during a marine heatwave.

Alternative splicing is a molecular mechanism that enables a single gene to encode multiple transcripts and proteins by post-transcriptional modification of pre-RNA molecules. Changes in the splicing scheme of genes can lead to modifications of the transcriptome and the proteome. This mechanism can enable organisms to respond to environmental fluctuations. In this study, we investigated patterns of alternative splicing in the liver of the coral reef fish Acanthochromis polyacanthus in response to the 2016 marine heatwave on the Great Barrier Reef. The differentially spliced (DS; n = 40) genes during the onset of the heatwave (i.e., 29.49°C or +1°C from average) were related to essential cellular functions such as the MAPK signaling system, Ca(2+) binding, and homeostasis. With the persistence of the heatwave for a period of one month (February to March), 21 DS genes were detected, suggesting that acute warming during the onset of the heatwave is more influential on alternative splicing than the continued exposure to elevated temperatures. After the heatwave, the water temperature cooled to ~24.96°C, and fish showed differential splicing of genes related to cyto-protection and post-damage recovery (n = 26). Two-thirds of the DS genes detected across the heatwave were also differentially expressed, revealing that the two molecular mechanisms act together in A. polyacanthus to cope with the acute thermal change. This study exemplifies how splicing patterns of a coral reef fish can be modified by marine heatwaves. Alternative splicing could therefore be a potential mechanism to adjust cellular physiological states under thermal stress and aid coral reef fishes in their response to more frequent acute thermal fluctuations in upcoming decades.

Molecular basis of parental contributions to the behavioural tolerance of elevated pCO2 in a coral reef fish.

Knowledge of adaptive potential is crucial to predicting the impacts of ocean acidification (OA) on marine organisms. In the spiny damselfish, Acanthochromis polyacanthus, individual variation in behavioural tolerance to elevated pCO2 has been observed and is associated with offspring gene expression patterns in the brain. However, the maternal and paternal contributions of this variation are unknown. To investigate parental influence of behavioural pCO2 tolerance, we crossed pCO2-tolerant fathers with pCO2-sensitive mothers and vice versa, reared their offspring at control and elevated pCO2 levels, and compared the juveniles' brain transcriptional programme. We identified a large influence of parental phenotype on expression patterns of offspring, irrespective of environmental conditions. Circadian rhythm genes, associated with a tolerant parental phenotype, were uniquely expressed in tolerant mother offspring, while tolerant fathers had a greater role in expression of genes associated with histone binding. Expression changes in genes associated with neural plasticity were identified in both offspring types: the maternal line had a greater effect on genes related to neuron growth while paternal influence impacted the expression of synaptic development genes. Our results confirm cellular mechanisms involved in responses to varying lengths of OA exposure, while highlighting the parental phenotype's influence on offspring molecular phenotype.

The time course of molecular acclimation to seawater in a euryhaline fish.

The Arabian pupfish, Aphanius dispar, is a euryhaline fish inhabiting both inland nearly-freshwater desert ponds and highly saline Red Sea coastal lagoons of the Arabian Peninsula. Desert ponds and coastal lagoons, located respectively upstream and at the mouths of dry riverbeds ("wadies"), have been found to potentially become connected during periods of intense rainfall, which could allow the fish to migrate between these different habitats. Flash floods would therefore flush Arabian pupfish out to sea, requiring a rapid acclimation to a greater than 40 ppt change in salinity. To investigate the molecular pathways of salinity acclimation during such events, a Red Sea coastal lagoon and a desert pond population were sampled, with the latter exposed to a rapid increase in water salinity. Changes in branchial gene expression were investigated via genome-wide transcriptome measurements over time from 6 h to 21 days. The two natural populations displayed basal differences in genes related to ion transport, osmoregulation and immune system functions. These mechanisms were also differentially regulated in seawater transferred fish, revealing their crucial role in long-term adaptation. Other processes were only transiently activated shortly after the salinity exposure, including cellular stress response mechanisms, such as molecular chaperone synthesis and apoptosis. Tissue remodelling processes were also identified as transient, but took place later in the timeline, suggesting their importance to long-term acclimation as they likely equip the fish with lasting adaptations to their new environment. The alterations in branchial functional pathways displayed by Arabian pupfish in response to salinity increases are diverse. These reveal a large toolkit of molecular processes important for adaptation to hyperosmolarity that allow for successful colonization to a wide variety of different habitats.

Diel pCO2 fluctuations alter the molecular response of coral reef fishes to ocean acidification conditions.

Environmental partial pressure of CO2 (pCO2 ) variation can modify the responses of marine organisms to ocean acidification, yet the underlying mechanisms for this effect remain unclear. On coral reefs, environmental pCO2  fluctuates on a regular day-night cycle. Effects of future ocean acidification on coral reef fishes might therefore depend on their response to this diel cycle of pCO2 . To evaluate the effects on the brain molecular response, we exposed two common reef fishes (Acanthochromis polyacanthus and Amphiprion percula) to two projected future pCO2  levels (750 and 1,000 µatm) under both stable and diel fluctuating conditions. We found a common signature to stable elevated pCO2 for both species, which included the downregulation of immediate early genes, indicating lower brain activity. The transcriptional programme was more strongly affected by higher average pCO2 in a stable treatment than for fluctuating treatments, but the largest difference in molecular response was between stable and fluctuating pCO2 treatments. This indicates that a response to a change in environmental pCO2 conditions is different for organisms living in a fluctuating than in stable environments. This differential regulation was related to steroid hormones and circadian rhythm (CR). Both species exhibited a marked difference in the expression of CR genes among pCO2 treatments, possibly accommodating a more flexible adaptive approach in the response to environmental changes. Our results suggest that environmental pCO2  fluctuations might enable reef fishes to phase-shift their clocks and anticipate pCO2 changes, thereby avoiding impairments and more successfully adjust to ocean acidification conditions.

Natural CO2 seeps reveal adaptive potential to ocean acidification in fish.

Volcanic CO2 seeps are natural laboratories that can provide insights into the adaptation of species to ocean acidification. While many species are challenged by reduced-pH levels, some species benefit from the altered environment and thrive. Here, we explore the molecular mechanisms of adaptation to ocean acidification in a population of a temperate fish species that experiences increased population sizes under elevated CO2. Fish from CO2 seeps exhibited an overall increased gene expression in gonad tissue compared with those from ambient CO2 sites. Up-regulated genes at CO2 seeps are possible targets of adaptive selection as they can directly influence the physiological performance of fishes exposed to ocean acidification. Most of the up-regulated genes at seeps were functionally involved in the maintenance of pH homeostasis and increased metabolism, and presented a deviation from neutral evolution expectations in their patterns of DNA polymorphisms, providing evidence for adaptive selection to ocean acidification. The targets of this adaptive selection are likely regulatory sequences responsible for the increased expression of these genes, which would allow a fine-tuned physiological regulation to maintain homeostasis and thrive at CO2 seeps. Our findings reveal that standing genetic variation in DNA sequences regulating the expression of genes in response to a reduced-pH environment could provide for adaptive potential to near-future ocean acidification in fishes. Moreover, with this study we provide a forthright methodology combining transcriptomics and genomics, which can be applied to infer the adaptive potential to different environmental conditions in wild marine populations.

Probing SWATH-MS as a tool for proteome level quantification in a nonmodel fish.

Quantitative proteomics via mass spectrometry can provide valuable insight into molecular and phenotypic characteristics of a living system. Recent mass spectrometry developments include data-independent acquisition (SWATH/DIA-MS), an accurate, sensitive and reproducible method for analysing the whole proteome. The main requirement for this method is the creation of a comprehensive spectral library. New technologies have emerged producing larger and more accurate species-specific libraries leading to a progressive collection of proteome references for multiple molecular model species. Here, for the first time, we set out to compare different spectral library constructions using multiple tissues from a coral reef fish to demonstrate its value and feasibility for nonmodel organisms. We created a large spectral library composed of 12,553 protein groups from liver and brain tissues. Via identification of differentially expressed proteins under fish exposure to elevated pCO2 and temperature, we validated the application and usefulness of these different spectral libraries. Successful identification of significant differentially expressed proteins from different environmental exposures occurred using the library with a combination of data-independent and data-dependent acquisition methods as well as both tissue types. Further analysis revealed expected patterns of significantly up-regulated heat shock proteins in a dual condition of ocean warming and acidification indicating the biological accuracy and relevance of the method. This study provides the first reference spectral library for a nonmodel organism. It represents a useful guide for future building of accurate spectral library references in nonmodel organisms allowing the discovery of ecologically relevant changes in the proteome.

Species-specific molecular responses of wild coral reef fishes during a marine heatwave.

The marine heatwave of 2016 was one of the longest and hottest thermal anomalies recorded on the Great Barrier Reef, influencing multiple species of marine ectotherms, including coral reef fishes. There is a gap in our understanding of what the physiological consequences of heatwaves in wild fish populations are. Thus, in this study, we used liver transcriptomes to understand the molecular response of five species to the 2016 heatwave conditions. Gene expression was species specific, yet we detected overlap in functional responses associated with thermal stress previously reported in experimental setups. The molecular response was also influenced by the duration of exposure to elevated temperatures. This study highlights the importance of considering the effects of extreme warming events when evaluating the consequences of climate change on fish communities.

Neural effects of elevated CO2 in fish may be amplified by a vicious cycle.

Maladaptive behavioural disturbances have been reported in some fishes and aquatic invertebrates exposed to projected future CO2 levels. These disturbances have been linked to altered ion gradients and neurotransmitter function in the brain. Still, it seems surprising that the relatively small ionic changes induced by near-future CO2 levels can have such profound neural effects. Based on recent transcriptomics data, we propose that a vicious cycle can be triggered that amplifies the initial disturbance, explaining how small pH regulatory adjustments in response to ocean acidification can lead to major behavioural alterations in fish and other water-breathing animals. The proposed cycle is initiated by a reversal of the function of some inhibitory GABAA receptors in the direction of neural excitation and then amplified by adjustments in gene expression aimed at suppressing the excitation but in reality increasing it. In addition, the increased metabolic production of CO2 by overexcited neurons will feed into the cycle by elevating intracellular bicarbonate levels that will lead to increased excitatory ion fluxes through GABAA receptors. We also discuss the possibility that an initiation of a vicious cycle could be one of the several factors underlying the differences in neural sensitivity to elevated CO2 displayed by fishes.

Beyond buying time: the role of plasticity in phenotypic adaptation to rapid environmental change.

How populations and species respond to modified environmental conditions is critical to their persistence both now and into the future, particularly given the increasing pace of environmental change. The process of adaptation to novel environmental conditions can occur via two mechanisms: (1) the expression of phenotypic plasticity (the ability of one genotype to express varying phenotypes when exposed to different environmental conditions), and (2) evolution via selection for particular phenotypes, resulting in the modification of genetic variation in the population. Plasticity, because it acts at the level of the individual, is often hailed as a rapid-response mechanism that will enable organisms to adapt and survive in our rapidly changing world. But plasticity can also retard adaptation by shifting the distribution of phenotypes in the population, shielding it from natural selection. In addition to which, not all plastic responses are adaptive-now well-documented in cases of ecological traps. In this theme issue, we aim to present a considered view of plasticity and the role it could play in facilitating or hindering adaption to environmental change. This introduction provides a re-examination of our current understanding of the role of phenotypic plasticity in adaptation and sets the theme issue's contributions in their broader context. Four key themes emerge: the need to measure plasticity across both space and time; the importance of the past in predicting the future; the importance of the link between plasticity and sexual selection; and the need to understand more about the nature of selection on plasticity itself. We conclude by advocating the need for cross-disciplinary collaborations to settle the question of whether plasticity will promote or retard species' rates of adaptation to ever-more stressful environmental conditions. This article is part of the theme issue 'The role of plasticity in phenotypic adaptation to rapid environmental change'.

Finding Nemo's Genes: A chromosome-scale reference assembly of the genome of the orange clownfish Amphiprion percula.

The iconic orange clownfish, Amphiprion percula, is a model organism for studying the ecology and evolution of reef fishes, including patterns of population connectivity, sex change, social organization, habitat selection and adaptation to climate change. Notably, the orange clownfish is the only reef fish for which a complete larval dispersal kernel has been established and was the first fish species for which it was demonstrated that antipredator responses of reef fishes could be impaired by ocean acidification. Despite its importance, molecular resources for this species remain scarce and until now it lacked a reference genome assembly. Here, we present a de novo chromosome-scale assembly of the genome of the orange clownfish Amphiprion percula. We utilized single-molecule real-time sequencing technology from Pacific Biosciences to produce an initial polished assembly comprised of 1,414 contigs, with a contig N50 length of 1.86 Mb. Using Hi-C-based chromatin contact maps, 98% of the genome assembly were placed into 24 chromosomes, resulting in a final assembly of 908.8 Mb in length with contig and scaffold N50s of 3.12 and 38.4 Mb, respectively. This makes it one of the most contiguous and complete fish genome assemblies currently available. The genome was annotated with 26,597 protein-coding genes and contains 96% of the core set of conserved actinopterygian orthologs. The availability of this reference genome assembly as a community resource will further strengthen the role of the orange clownfish as a model species for research on the ecology and evolution of reef fishes.

An interplay between plasticity and parental phenotype determines impacts of ocean acidification on a reef fish.

The impacts of ocean acidification will depend on the ability of marine organisms to tolerate, acclimate and eventually adapt to changes in ocean chemistry. Here, we use a unique transgenerational experiment to determine the molecular response of a coral reef fish to short-term, developmental and transgenerational exposure to elevated CO2, and to test how these responses are influenced by variations in tolerance to elevated CO2 exhibited by the parents. Within-generation responses in gene expression to end-of-century predicted CO2 levels indicate that a self-amplifying cycle in GABAergic neurotransmission is triggered, explaining previously reported neurological and behavioural impairments. Furthermore, epigenetic regulator genes exhibited a within-generation specific response, but with some divergence due to parental phenotype. Importantly, we find that altered gene expression for the majority of within-generation responses returns to baseline levels following parental exposure to elevated CO2 conditions. Our results show that both parental variation in tolerance and cross-generation exposure to elevated CO2 are crucial factors in determining the response of reef fish to changing ocean chemistry.

Impact of life history traits on gene flow: A multispecies systematic review across oceanographic barriers in the Mediterranean Sea.

BACKGROUND: Marine species can demonstrate strong genetic differentiation and population structure despite the hypothesis of open seas and high connectivity. Some suggested drivers causing the genetic breaks are oceanographic barriers and the species' biology. We assessed the relevance of seven major oceanographic fronts on species connectivity while considering their dispersal capacity and life strategy. METHODS: We systematically reviewed the scientific articles reporting population genetic differentiation along the Mediterranean Sea and across the Atlantic-Mediterranean transition. We retained those considering at least one sampling locality at each side of an oceanographic front, and at least two localities with no-front between them to correctly assess the effect of the front. To estimate the impact of life history characteristics affecting connectivity we considered the planktonic larval duration (PLD) and adult life strategy. RESULTS: Oceanographic barriers in the Mediterranean Sea seem to reduce gene flow globally; however, this effect is not homogeneous considering the life history traits of the species. The effect of the oceanographic fronts reduces gene flow in highly mobile species with PLD larger than 2-4 weeks. Benthic sessile species and/or with short PLD (< 2 weeks) have more significant genetic breaks between localities than species with higher motility; however, genetic differentiation occurs independently of the presence of a front. CONCLUSION: Genetic connectivity is important for populations to recover from anthropogenic or natural impacts. We show that species with low mobility, mostly habitat-formers, have high genetic differentiation but low gene flow reduction mediated by the front, therefore, considering the importance of these species, we emphasize the vulnerability of the Mediterranean ecosystems and the necessity of protection strategies based on the whole ecosystem.