Several recent high intensity ENSO events have caused strong negative impacts on the adult phases of foundational species in coral reef ecosystems, but comparatively little is known about how climatic variables related to recent ENSOs are impacting the supply of larvae to benthic populations. In marine fishes and invertebrates, reproductive adults and planktonic larvae are generally more sensitive to environmental variability than older, non-reproductive adults. Further, the transport of larvae in ocean currents may also be strongly ENSO dependent. The interactions between the dynamics of larval survivorship and larval transport could lead to population bottlenecks as stronger ENSO events become more common. We tested the predictions of this hypothesis around the Main Hawaiian Islands (MHI) by constructing a correlation matrix of physical and biological time series variables that spanned 11 years (2007-2017) and multiple ENSO events. Our correlation matrix included four types of variables: i. published ENSO indices, ii. satellite-derived sea surface temperature (SST) and chlorophyll variables, iii. abundance and diversity of larval fishes sampled during the late winter spawning season off Oahu, and iv. abundance and diversity of coral reef fish recruits sampled on the western shore of the Big Island of Hawaii. We found that the abundance and diversity of larval fishes was negatively correlated with the Multivariate El Ni & ntilde;o Index (MEI), and that larval variables were positively correlated with measures of fall recruitment (September & November), but not correlated with spring-summer recruitment (May & July). In the MHI, SST variables were not correlated with the MEI, but two successive El Ni & ntilde;o events of 2014-15 and 2015-2016 were characterized by SST maxima approaching 30 degrees C. Two large pulses of benthic recruitment occurred in the 2009 and 2014 recruitment seasons, with > 8000 recruits observed by divers over the summer and fall months. Both events were characterized by either neutral or negative MEI indices measured during the preceding winter months. These patterns suggest that La Ni & ntilde;a and the neutral phases of the ENSO cycle are generally favorable for adult reproduction and larval development in the spring and summer, while El Ni & ntilde;o phases may limit recruitment in the late summer and fall. We hypothesize that episodic recruitment during non-El Ni & ntilde;o phases is related to favorable survivorship and transport dynamics that are associated with the formation of pairs of anticyclonic and cyclonic eddies on the leeward sides (western shores) of the Main Hawaiian Islands.

Scleractinian corals are the main modern builders of coral reefs, which are major hot spots of marine biodiversity. Southern Atlantic reef corals are understudied compared to their Caribbean and Indo-Pacific counterparts and many hypotheses about their population dynamics demand further testing. We employed thousands of single nucleotide polymorphisms (SNPs) recovered via ezRAD to characterize genetic population structuring and species boundaries in the amphi-Atlantic hard coral genus Favia. Coalescent-based species delimitation (BFD* - Bayes Factor Delimitation) recovered F. fragum and F. gravida as separate species. Although our results agree with depth-related genetic structuring in F. fragum, they did not support incipient speciation of the 'tall' and 'short' morphotypes. The preferred scenario also revealed a split between two main lineages of F. gravida, one from Ascension Island and the other from Brazil. The Brazilian lineage is further divided into a species that occurs throughout the Northeastern coast and another that ranges from the Abrolhos Archipelago to the state of Espirito Santo. BFD* scenarios were corroborated by analyses of SNP matrices with varying levels of missing data and by a speciation-based delimitation approach (DELINEATE). Our results challenge current notions about Atlantic reef corals because they uncovered surprising genetic diversity in Favia and rejected the long-standing hypothesis that Abrolhos Archipelago may have served as a Pleistocenic refuge during the last glaciations.

A major challenge in biodiversity research is the incorporation of species interactions into frameworks describing population and community response to global edfnmental change (GEC). Mutualisms are a type of species interaction especially sensitive to changing environmental conditions, and the breakdown of facilitative species interactions could amplify the negative impacts of novel climate regimes on focal species. Here, we investigate how reciprocal interactions between two coastal foundation species, the eastern oyster (Crassostrea virginica) and eelgrass (Zostera marina) shift in sign and magnitude in response to ocean warming (+1.5 degrees C) and acidification (-0.4 pH) via a manipulative co-culture experiment in mesocosms. Under ambient environmental conditions, oysters facilitated eelgrass leaf growth and clonal reproduction by 35% and 38%, respectively. Simultaneously, eelgrass decreased the oyster condition index (the ratio of tissue to shell biomass) by 35%, indicating greater allocation of energy to shell growth instead of soft tissues at ambient conditions. Varying sensitivities of each species to ocean warming and/or acidification treatments led to complex shifts in species interactions that were trait dependent. As such, community outcomes under future conditions were influenced by species interactions that amplified and mitigated species response to environmental change. Synthesis: Given that species interaction effect sizes were similar in magnitude to effect sizes of warming or pH treatments, our results underscore the need to identify key species and interaction types that strongly influence community response to GEC. Specifically, for macrophyte-bivalve interactions, understanding how physiological limitations on growth are impacted by environmental heterogeneity and co-culture will support the successful restoration of natural populations and the rapid expansion of aquaculture.

Northern sand lance (Ammodytes dubius) are essential forage fish in most offshore, temperate-to-polar waters on the Northwest Atlantic shelf (NWA), but their population structure and genetic separation from the American sand lance (A. americanus) remain unresolved. We assembled a reference genome for A. dubius (first in the Ammodytidae) and then used low-coverage whole genome sequencing on 262 specimens collected across the species distribution (Mid-Atlantic Bight to Greenland) to quantify genetic differentiation between geographic regions based on single nucleotide polymorphisms. We found strong separation between A. dubius from locations north and south of the Scotian Shelf, largely due to massive genetic differentiation spanning most of chromosomes 21 and 24. Genetic distance increased with geographic distance in the smaller southern cluster but not in the larger northern cluster, where genetic homogeneity appeared across large geographic distances (>10(3) km). The two genetic clusters coincide with a clear break in winter sea surface temperature, suggesting that differential offspring survival, rather than limited transport, causes a break in realized connectivity. Nuclear and mitochondrial DNA both clearly delineated A. dubius from A. americanus, thereby confirming a species boundary through spatial niche partitioning into inshore (A. americanus) and offshore (A. dubius) sand lance species on the NWA.

Cryptic and hybridizing species may lack diagnostic taxonomic characters leaving researchers with semi-diagnostic ones. Identification based on such characters is probabilistic, the probability of correct identification depending on the species composition in a mixed population. Here we test the possibilities of applying a semi-diagnostic conchological character for distinguishing two cryptic species of blue mussels, Mytilus edulis and M. trossulus. These ecologically, stratigraphically and economically important molluscs co-occur and hybridize in many areas of the North Atlantic and the neighboring Arctic. Any cues for distinguishing them in sympatry without genotyping would save much research effort. Recently these species have been shown to statistically differ in the White Sea, where a simple character of the shell was used to distinguish two mussel morphotypes. In this paper, we analyzed the associations between morphotypes and species-specific genotypes based on an abundant material from the waters of the Kola Peninsula (White Sea, Barents Sea) and a more limited material from Norway, the Baltic Sea, Scotland and the Gulf of Maine. The performance of the “morphotype test” for species identification was formally evaluated using approaches from evidence-based medicine. Interspecific differences in the morphotype frequencies were ubiquitous and unidirectional, but their scale varied geographically (from 75% in the White Sea to 15% in the Baltic Sea). In addition, salinity-related variation of this character within M. edulis was revealed in the Arctic Barents Sea. For every studied region, we established relationships between the proportions of the morphotypes in the populations as well as between the proportions of the morphotypes in samples and the probabilities of mussels of different morphotypes being M. trossulus and M. edulis. We provide recommendations for the application of the morphotype test to mussels from unstudied contact zones and note that they may apply equally well to other taxa identified by semi-diagnostic traits.

Background In the Tropical Eastern Pacific (TEP), four species of parrotfishes with complex phylogeographic histories co-occur in sympatry on rocky reefs from Baja California to Ecuador: Scarus compressus , S. ghobban , S. perrico , and S. rubroviolaceus . The most divergent, S. perrico , separated from a Central Indo-Pacific ancestor in the late Miocene (6.6 Ma). We tested the hypothesis that S. compressus was the result of ongoing hybridization among the other three species by sequencing four nuclear markers and a mitochondrial locus in samples spanning 2/3 of the latitudinal extent of the TEP. Results A Structure model indicated that K = 3 fit the nuclear data and that S. compressus individuals had admixed genomes. Our data could correctly detect and assign pure adults and F1 hybrids with > 0.90 probability, and correct assignment of F2s was also high in some cases. NewHybrids models revealed that 89.8% (n = 59) of the S. compressus samples were F1 hybrids between either S. perrico × S. ghobban or S. perrico × S. rubroviolaceus . Similarly, the most recently diverged S. ghobban and S. rubroviolaceus were hybridizing in small numbers, with half of the admixed individuals assigned to F1 hybrids and the remainder likely > F1 hybrids. We observed strong mito-nuclear discordance in all hybrid pairs. Migrate models favored gene flow between S. perrico and S. ghobban , but not other species pairs. Conclusions Mating between divergent species is giving rise to a region-wide, multispecies hybrid complex, characterized by a high frequency of parental and F1 genotypes but a low frequency of > F1 hybrids. Trimodal structure, and evidence for fertility of both male and female F1 hybrids, suggest that fitness declines sharply in later generation hybrids. In contrast, the hybrid population of the two more recently diverged species had similar frequencies of F1 and > F1 hybrids, suggesting accelerating post-mating incompatibility with time. Mitochondrial genotypes in hybrids suggest that indiscriminate mating by male S. perrico is driving pre-zygotic breakdown, which may reflect isolation of this endemic species for millions of years resulting in weak selection for conspecific mate recognition. Despite overlapping habitat use and high rates of hybridization, species boundaries are maintained by a combination of pre- and post-mating processes in this complex.

Inbreeding is a potent evolutionary force shaping the distribution of genetic variation within and among populations of plants and animals. Yet, our understanding of the forces shaping the expression and evolution of nonrandom mating in general, and inbreeding in particular, remains remarkably incomplete. Most research on plant mating systems focuses on self-fertilization and its consequences for automatic selection, inbreeding depression, purging, and reproductive assurance, whereas studies of animal mating systems have often assumed that inbreeding is rare, and that natural selection favors traits that promote outbreeding. Given that many sessile and sedentary marine invertebrates and marine macroalgae share key life history features with seed plants (e.g., low mobility, modular construction, and the release of gametes into the environment), their mating systems may be similar. Here, we show that published estimates of inbreeding coefficients (FIS ) for sessile and sedentary marine organisms are similar and at least as high as noted in terrestrial seed plants. We also found that variation in FIS within invertebrates is related to the potential to self-fertilize, disperse, and choose mates. The similarity of FIS for these organismal groups suggests that inbreeding could play a larger role in the evolution of sessile and sedentary marine organisms than is currently recognized. Specifically, associations between traits of marine invertebrates and FIS suggest that inbreeding could drive evolutionary transitions between hermaphroditism and separate sexes, direct development and multiphasic life cycles, and external and internal fertilization.

The biogeochemistry of the Gulf of Maine (GOM) is rapidly changing in response to the changing climate, including rising temperatures, acidification, and declining primary productivity. These impacts are projected to worsen over the next 100 y and will apply selective pressure on populations of marine calcifiers. This study investigates the transcriptome expression response to these changes in ecologically and economically important marine calcifiers, blue mussels. Wild mussels (Mytilus edulis and Mytilus trossulus) were sampled from sites spanning the GOM and exposed to two different biogeochemical water conditions: (1) present-day conditions in the GOM and (2) simulated future conditions, which included elevated temperature, increased acidity, and decreased food supply. Patterns of gene expression were measured using RNA sequencing from 24 mussel samples and contrasted between ambient and future conditions. The net calcification rate, a trait predicted to be under climate-induced stress. was measured for each individual over a 2-wk exposure period and used as a covariate along with gene expression patterns. Generalized linear models, with and without the calcification rate, were used to identify differentially expressed transcripts between ambient and future conditions. The comparison revealed transcripts that likely comprise a core stress response characterized by the induction of molecular chaperones, genes involved in aerobic metabolism, and indicators of cellular stress. Furthermore, the model contrasts revealed transcripts that may be associated with individual variation in calcification rate and suggest possible biological processes that may have downstream effects on calcification phenotypes, such as zinc-ion binding and protein degradation. Overall, these findings contribute to the understanding of blue mussel adaptive responses to imminent climate change and suggest metabolic pathways are resilient in variable environments.

ABSTRACT Hybrid zones provide natural experiments in recombination within and between genomes that may have strong effects on organismal fitness. On the East Coast of North America, two distinct lineages of the European green crab (Carcinus maenas) have been introduced in the last two centuries. These two lineages with putatively different adaptive properties have hybridized along the coast of the eastern Gulf of Maine, producing new nuclear and mitochondrial combinations that show clinal variation correlated with water temperature. To test the hypothesis that mitochondrial or nuclear genes have effects on thermal tolerance, we first measured the response to cold stress in crabs collected throughout the hybrid zone, then sequenced the mitochondrial CO1 gene and two nuclear single nucleotide polymorphisms (SNPs) representative of nuclear genetic lineage. Mitochondrial haplotype had a strong association with the ability of crabs to right themselves at 4.5°C that was sex specific: haplotypes originally from northern Europe gave male crabs an advantage while there was no haplotype effect on righting in female crabs. By contrast, the two nuclear SNPs that were significant outliers in a comparison between northern and southern C. maenas populations had no effect on righting response at low temperature. These results add C. maenas to the shortlist of ectotherms in which mitochondrial variation has been shown to affect thermal tolerance, and suggest that natural selection is shaping the structure of the hybrid zone across the Gulf of Maine. Our limited genomic sampling does not eliminate the strong possibility that mito-nuclear co-adaptation may play a role in the differences in thermal phenotypes documented here. Linkage between mitochondrial genotype and thermal tolerance suggests a role for local adaptation in promoting the spread of invasive populations of C. maenas around the world.

Several shell diseases are impacting a variety of decapod crustaceans in southern New England, but have rarely been reported in the colder waters of the eastern Gulf of Maine. Here we document a possible outbreak of shell disease impacting Cancer borealis (Jonah Crab) on Kent Island, NB, Canada. On low tides of 31 August 31-3 September 2017 we found hundreds of Jonah Crabs stranded above the tide line and resting on top of the dense canopies of fucoid algae. Closer inspection of exoskeletons revealed the clinical signs of classical shell disease: dark circular patches and lesions that penetrated the cuticle. A sample of 30 stranded Jonah Crabs revealed that 28 (93%) were adult females. On the next low tide, we found the same pattern of exposed Jonah Crabs and observed numerous instances of Lams smithsonianus (Herring Gull) predation. Continuous monitoring of shallow-water temperatures over the last 3 years revealed that average daily summer temperatures have been regularly exceeding a shell-disease threshold of 12 degrees C on Kent Island. Between 13 September and 31 October 2015 there were 19 days with an average water temperature above 12 degrees C and 43 days during the same interval in 2016.

A key component to understanding the evolutionary response to a changing climate is linking underlying genetic variation to phenotypic variation in stress response. Here, we use a genome-wide association approach (GWAS) to understand the genetic architecture of calcification rates under simulated climate stress. We take advantage of the genomic gradient across the blue mussel hybrid zone (Mytilus edulis and Mytilus trossulus) in the Gulf of Maine (GOM) to link genetic variation with variance in calcification rates in response to simulated climate change. Falling calcium carbonate saturation states are predicted to negatively impact many marine organisms that build calcium carbonate shells - like blue mussels. We sampled wild mussels and measured net calcification phenotypes after exposing mussels to a climate change' common garden, where we raised temperature by 3 degrees C, decreased pH by 0.2 units and limited food supply by filtering out planktonic particles >5m, compared to ambient GOM conditions in the summer. This climate change exposure greatly increased phenotypic variation in net calcification rates compared to ambient conditions. We then used regression models to link the phenotypic variation with over 170000 single nucleotide polymorphism loci (SNPs) generated by genotype by sequencing to identify genomic locations associated with calcification phenotype, and estimate heritability and architecture of the trait. We identified at least one of potentially 2-10 genomic regions responsible for 30% of the phenotypic variation in calcification rates that are potential targets of natural selection by climate change. Our simulations suggest a power of 13.7% with our study's average effective sample size of 118 individuals and rare alleles, but a power of >90% when effective sample size is 900.

Reef-fish management and conservation is hindered by a lack of information on fish populations prior to large-scale contemporary human impacts. As a result, relatively pristine sites are often used as conservation baselines for populations near sites affected by humans. This space-for-time approach can only be validated by sampling assemblages through time. We used archaeological remains to evaluate whether the remote, uninhabited Northwestern Hawaiian Islands (NWHI) might provide a reasonable proxy for a lightly exploited baseline in the Main Hawaiian Islands (MHI). We used molecular and morphological techniques to describe the taxonomic and size composition of the scarine parrotfish catches present in 2 archaeological assemblages from the MHI, compared metrics of these catches with modern estimates of reproductive parameters to evaluate whether catches represented by the archaeological material were consistent with sustainable fishing, and evaluated overlap between size structures represented by the archaeological material and modern survey data from the MHI and the NWHI to assess whether a space-for-time substitution is reasonable. The parrotfish catches represented by archaeological remains were consistent with sustainable fishing because they were dominated by large, mature individuals whose average size remained stable from prehistoric (AD approximately 1400-1700) through historic (AD 1700-1960) periods. The ancient catches were unlike populations in the MHI today. Overlap between the size structure of ancient MHI catches and modern survey data from the NWHI or the MHI was an order of magnitude greater for the NWHI comparison, a result that supports the validity of using the NWHI parrotfish data as a proxy for the MHI before accelerated, heavy human impacts in modern times.

Although holoplankton are ocean drifters and exhibit high dispersal potential, a number of studies on single species are finding highly divergent genetic clades. These cryptic species complexes are important to discover and describe, as identification of common marine species is fundamental to understanding ecosystem dynamics. Here we investigate the global diversity within Pleuromamma piseki and P. gracilis, two dominant members of the migratory zooplankton assemblage in subtropical and tropical waters worldwide. Using DNA sequence data from the mitochondrial gene cytochrome c oxidase subunit II (mtCOII) from 522 specimens collected across the Pacific, Atlantic and Indian Oceans, we discover twelve well-resolved genetically distinct clades in this species complex (Bayesian posterior probabilities >0.7; 6.3-17% genetic divergence between clades). The morphologically described species P. piseki and P. gracilis did not form monophyletic groups, rather they were distributed throughout the phylogeny and sometimes co-occurred within well-resolved clades: this result suggests that morphological characters currently used for taxonomic identification of P. gracilis and P. piseki may be inaccurate as indicators of species' boundaries. Cryptic clades within the species complex ranged from being common to rare, and from cosmopolitan to highly restricted in distribution across the global ocean. These novel lineages appear to be ecologically divergent, with distinct biogeographic distributions across varied pelagic habitats. We hypothesize that these mtDNA lineages are distinct species and suggest that resolving their systematic status is important, given the ecological significance of the genus Pleuromamma in subtropical-tropical waters worldwide.

AimTo explore the spatial and temporal genetic structure of four tropical hermit crabs in the genus Calcinus with varying habitat use in order to test for impacts of sea-level change and demography in shaping contemporary population structure and to understand how this structure relates to the process of speciation in the genus.LocationCentral Pacific.MethodsWe sequenced 586bp of the cytochrome c oxidase subunit I gene (COI) (n=702) and analysed the data for population differentiation and demographic changes. We complemented the sequences with abundance surveys of targeted species and modelled potential habitat availability in response to sea-level change.ResultsSequence data revealed high haplotype diversity (h=0.685-0.983) and low nucleotide diversity (=0.002-0.018) for all species. There was little population differentiation and extensive geographical haplotype sharing within all species, despite dramatic shifts in the abundance of species among locations, which appear to result from ecological interactions rather than limits to contemporary larval dispersal. Population expansion occurred most recently in the subtidal species Calcinushaigae (30-70ka), whereas the intertidal species showed earlier expansions: Calcinusseurati: 110-140ka, and Calcinuslaevimanus: 220-250ka. Differences in timing can be linked to the prediction that subtidal habitat area is strongly affected by changing sea level, while intertidal habitat area is affected less strongly. Interestingly, unlike the West Pacific, habitat in the Central Pacific remains relatively equidistant.Main conclusionsHabitat availability during sea-level fluctuations, rather than dispersal limitation per se, appears to be a potential force shaping the population genetic patterns of subtidal species, and perhaps speciation of tropical Calcinus hermit crabs. Insofar as this represents a general pattern, historical sea-level change may play a role in structuring Central Pacific reef species through alteration of habitat availability rather than isolation and vicariance.

Even with well-known sampling biases, the fossil record is key to understanding macro-evolutionary patterns. During the Miocene to Pleistocene in the Caribbean Sea, the fossil record of scleractinian corals shows a remarkable period of rapid diversification followed by massive extinction. Here we combine a time-calibrated molecular phylogeny based on three nuclear introns with an updated fossil stratigraphy to examine patterns of radiation and extinction in Caribbean corals within the traditional family Faviidae.

We used 15 microsatellite markers to estimate the selfing rate (s), outcrossing rate (tO) and hybridization between partially sympatric ecomorphs (tH) of the coral Favia fragum. Genotyping of progeny arrays revealed complete self-fertilization in the Tall ecomorph and low outcrossing (tO + tH < 1%) in the Short ecomorph. Further, all larvae could be assigned with high probability to the same population as their parental dam, indicating no hybridization between ecomorphs (tH = 0). Despite low ecological estimates of outcrossing, Q values from highly structured adult populations indicated that 9% of the adult samples were the products of outcrossing, and an additional 11% were hybrids. Reproductive isolation appears to have a strong geographical component, as we did not detect hybrids at a second site where the two ecomorphs were distributed in complete microallopatry. Adult estimates of gene flow within ecomorphs may be positively biased by ecomorph-specific patterns of inbreeding depression, but cryptic gene flow between ecomorphs is most likely explained by undetected outcrossing and the fact that hybrid lineages persist after repeated generations of self-fertilization. Our microsatellite data show that phenotypic differences between ecomorphs are maintained in sympatry despite evidence for hybridization.