Local and regional scale habitat heterogeneity contribute to genetic adaptation in a commercially important marine mollusc (Haliotis rubra) from southeastern Australia

Characterising adaptive genetic divergence among conspecific populations is often achieved by studying genetic variation across defined environmental gradients. In marine systems this is challenging due to a paucity of information on habitat heterogeneity at local and regional scales and a dependency on sampling regimes that are typically limited to broad longitudinal and latitudinal environmental gradients. As a result, the spatial scales at which selection processes operate and the environmental factors that contribute to genetic adaptation in marine systems are likely to be unclear. In this study we explore patterns of adaptive genetic structuring in a commercially‐ harvested abalone species (Haliotis rubra) from southeastern Australia, using a panel of genome‐wide SNP markers (5,239 SNPs), and a sampling regime informed by marine LiDAR bathymetric imagery and 20‐year hindcasted oceanographic models. Despite a lack of overall genetic structure across the sampling distribution, significant genotype associations with heterogeneous habitat features were observed at local and regional spatial scales, including associations with wave energy, ocean current, sea surface temperature, and geology. These findings provide insights into the potential resilience of the species to changing marine climates and the role of migration and selection on recruitment processes, with implications for conservation and fisheries management. This study points to the spatial scales at which selection processes operate in marine systems and highlights the benefits of geospatially‐informed sampling regimes for overcoming limitations associated with marine population genomic research.     

Seascape genomics reveals adaptive divergence in a connected and commercially important mollusc,the greenlip abalone (Haliotis laevigata), along a longitudinal environmental gradient

Populations of broadcast spawning marine organisms often have large sizes and are exposed to reduced genetic drift. Under such scenarios, strong selection associated with spatial environmental heterogeneity is expected to drive localized adaptive divergence, even in the face of connectivity. We tested this hypothesis using a seascape genomics approach in the commercially important greenlip abalone (Haliotis laevigata). We assessed how its population structure has been influenced by environmental heterogeneity along a zonal coastal boundary in southern Australia linked by strong oceanographic connectivity. Our data sets include 9,109 filtered SNPs for 371 abalones from 13 localities and environmental mapping across ~800 km. Genotype–environment association analyses and outlier tests defined 8,786 putatively neutral and 323 candidate adaptive loci. From a neutral perspective, the species is better represented by a metapopulation with very low differentiation (global F_ST = 0.0081) and weak isolation by distance following a stepping‐stone model. For the candidate adaptive loci, however, model‐based and model‐free approaches indicated five divergent population clusters. After controlling for spatial distance, the distribution of putatively adaptive variation was strongly correlated to selection linked to minimum sea surface temperature and oxygen concentration. Around 80 candidates were annotated to genes with functions related to high temperature and/or low oxygen tolerance, including genes that influence the resilience of abalone species found in other biogeographic regions. Our study includes a documented example about the uptake of genomic information in fisheries management and supports the hypothesis of adaptive divergence due to coastal environmental heterogeneity in a connected metapopulation of a broadcast spawner.     

Molecular genetics to inform spatial management in benthic invertebrate fisheries: a case study using the Australian Greenlip Abalone

Hierarchical sampling and subsequent microsatellite genotyping of >2300 Haliotis laevigata (greenlip abalone) from 19 locations distributed across five biogeographic regions have substantially advanced our knowledge of population structure and connectivity in this commercially important species. The study has found key differences in stock structure of H. laevigata compared with the sympatric and congeneric Haliotis rubra (blacklip abalone) and yielded valuable insights into the management of fisheries targeting species characterized by spatial structure at small scales (i.e. S‐fisheries). As with H. rubra, H. laevigata comprise a series of metapopulations with strong self‐recruitment. However, the spatial extent of H. laevigata metapopulations (reefal areas around 30 km²; distances of up to 135 km are effective barriers to larval dispersal) was substantially greater than that identified for H. rubra (Miller et al. 2009). Differences in the dynamics and scale of population processes, even between congeneric haliotids as made evident in this study, imply that for S‐fisheries, it is difficult to generalize about the potential consequences of life history commonalities. Consequently, species‐specific management reflective of the population structure of the target species remains particularly important. This will likely require integration of information about stock structure and connectivity with data on life history and population dynamics to determine the necessary input (e.g. number of fishers, fishing effort) and output (e.g. minimum legal size, total allowable catch) controls to underpin their sustainable management.     

Asymmetric oceanographic processes mediate connectivity and population genetic structure,as revealed by RADseq,in a highly dispersive marine invertebrate (Parastichopus californicus)

Marine populations are typically characterized by weak genetic differentiation due to the potential for long‐distance dispersal favouring high levels of gene flow. However, strong directional advection of water masses or retentive hydrodynamic forces can influence the degree of genetic exchange among marine populations. To determine the oceanographic drivers of genetic structure in a highly dispersive marine invertebrate, the giant California sea cucumber (Parastichopus californicus), we first tested for the presence of genetic discontinuities along the coast of North America in the northeastern Pacific Ocean. Then, we tested two hypotheses regarding spatial processes influencing population structure: (i) isolation by distance (IBD: genetic structure is explained by geographic distance) and (ii) isolation by resistance (IBR: genetic structure is driven by ocean circulation). Using RADseq, we genotyped 717 individuals from 24 sampling locations across 2,719 neutral SNPs to assess the degree of population differentiation and integrated estimates of genetic variation with inferred connectivity probabilities from a biophysical model of larval dispersal mediated by ocean currents. We identified two clusters separating north and south regions, as well as significant, albeit weak, substructure within regions (F_ST = 0.002, p = .001). After modelling the asymmetric nature of ocean currents, we demonstrated that local oceanography (IBR) was a better predictor of genetic variation (R² = .49) than geographic distance (IBD) (R² = .18), and directional processes played an important role in shaping fine‐scale structure. Our study contributes to the growing body of literature identifying significant population structure in marine systems and has important implications for the spatial management of P. californicus and other exploited marine species.     

Integrating population genetics and conservation biology in the era of genomics

As one of the final activities of the ESF-CONGEN Networking programme, a conference entitled ‘Integrating Population Genetics and Conservation Biology’ was held at Trondheim, Norway, from 23 to 26 May 2009. Conference speakers and poster presenters gave a display of the state-of-the-art developments in the field of conservation genetics. Over the five-year running period of the successful ESF-CONGEN Networking programme, much progress has been made in theoretical approaches, basic research on inbreeding depression and other genetic processes associated with habitat fragmentation and conservation issues, and with applying principles of conservation genetics in the conservation of many species. Future perspectives were also discussed in the conference, and it was concluded that conservation genetics is evolving into conservation genomics, while at the same time basic and applied research on threatened species and populations from a population genetic point of view continues to be emphasized.     

Establishing the evolutionary compatibility of potential sources of colonizers for overfished stocks: a population genomics approach

Identifying fish stock structure is fundamental to pinpoint stocks that might contribute colonizers to overfished stocks. However, a stock's potential to contribute to rebuilding hinges on demographic connectivity, a challenging parameter to measure. With genomics as a new tool, fisheries managers can detect signatures of natural selection and thus identify fishing areas likely to contribute evolutionarily compatible colonizers to an overfished area (i.e. colonizers that are not at a fitness disadvantage in the overfished area and able to reproduce at optimal rates). Identifying evolutionarily compatible stocks would help narrow the focus on establishing demographic connectivity where it matters. Here, we genotype 4723 SNPs in 616 orange roughy (Hoplostethus atlanticus) across five fishing areas off the Tasmanian coast in Australia. We ask whether these areas form a single genetic unit, and test for signatures of local adaptation. Results from amova , structure , discriminant analysis of principal components, bayesass and isolation by distance suggest that sampled locations are subjected to geneflow amounts that are above what is needed to establish ‘drift connectivity’. However, it remains unclear whether there is a single panmictic population or several highly connected populations. Most importantly, we did not find any evidence of local adaptation, suggesting that the examined orange roughy stocks are evolutionarily compatible. The data have helped test an assumption of the orange roughy management programme and to formulate hypotheses regarding stock demographic connectivity. Overall, our results demonstrate the potential of genomics to inform fisheries management, even when evidence for stock structure is sparse.     

Uncovering the genetic basis of adaptive change: on the intersection of landscape genomics and theoretical population genetics

A workshop recently held at the École Polytechnique Fédérale de Lausanne (EPFL, Switzerland) was dedicated to understanding the genetic basis of adaptive change, taking stock of the different approaches developed in theoretical population genetics and landscape genomics and bringing together knowledge accumulated in both research fields. Indeed, an important challenge in theoretical population genetics is to incorporate effects of demographic history and population structure. But important design problems (e.g. focus on populations as units, focus on hard selective sweeps, no hypothesis‐based framework in the design of the statistical tests) reduce their capability of detecting adaptive genetic variation. In parallel, landscape genomics offers a solution to several of these problems and provides a number of advantages (e.g. fast computation, landscape heterogeneity integration). But the approach makes several implicit assumptions that should be carefully considered (e.g. selection has had enough time to create a functional relationship between the allele distribution and the environmental variable, or this functional relationship is assumed to be constant). To address the respective strengths and weaknesses mentioned above, the workshop brought together a panel of experts from both disciplines to present their work and discuss the relevance of combining these approaches, possibly resulting in a joint software solution in the future.     

Parasites as indicators of movement and population connectivity of a non-diadromous, tropical estuarine teleost: king threadfin Polydactylus macrochir

Temporal and spatial patterns in parasite assemblages were examined to evaluate the degree of movement and connectivity of post-recruitment life-history stages of a large, non-diadromous tropical estuarine teleost, king threadfin Polydactylus macrochir, collected from 18 locations across northern Australia. Ten parasites types (juvenile stages of two nematodes and seven cestodes, and adults of an acanthocephalan) were deemed to be suitable for use as biological tags, in that they were considered to have a long residence time in the fish, were relatively easy to find and were morphologically very different to each other which aided discrimination. Univariate and discriminant function analysis of these parasites revealed little difference in temporal replicates collected from five locations, suggesting that the parasite communities were stable over the timeframes explored. Univariate, discriminant function, and Bray-Curtis similarity analyses indicated significant spatial heterogeneity, with Bray-Curtis classification accuracies ranging from 55 to 100% for locations in north-western and northern Australia, 24 to 88% in the Gulf of Carpentaria, and 39 to 88% on the east coast of Queensland. Few differences were observed among locations separated by <200 km. The observed patterns of parasite infection are in agreement with concurrent studies of movement and connectivity of P. macrochir in that they indicate a complex population structure across northern Australia. These results should be considered when reviewing the management arrangements for this species.     

The genomics of adaptation,divergence and speciation: a congealing theory

In this issue, Flaxman et al. ( 2014 ) report the results of sophisticated whole‐genome simulations of speciation with gene flow, enhancing our understanding of the process by building on previous single‐locus, multilocus and analytical works. Their findings provide us with new insights about how genomes can diverge and the importance of statistical and chromosomal linkage in facilitating reproductive isolation. The authors characterize the conditions under which, even with high gene flow and weak divergent selection, reproductive isolation between populations can occur due to the emergent stochastic process of genomewide congealing, where numerous statistically or physically linked loci of small effect allow selection to limit effective migration rates. The initial congealing event can occur within a broad range conditions, and once initiated, the self‐reinforcing process leads to rapid divergence and ultimately two reproductively isolated populations. Flaxman et al.'s ( 2014 ) work is a valuable contribution to our understanding of speciation with gene flow and in making a more predictive field of evolutionary genomics and speciation.     

Local adaptation and oceanographic connectivity patterns explain genetic differentiation of a marine diatom across the North Sea–Baltic Sea salinity gradient

Drivers of population genetic structure are still poorly understood in marine micro‐organisms. We exploited the North Sea–Baltic Sea transition for investigating the seascape genetics of a marine diatom, Skeletonema marinoi. Eight polymorphic microsatellite loci were analysed in 354 individuals from ten locations to analyse population structure of the species along a 1500‐km‐long salinity gradient ranging from 3 to 30 psu. To test for salinity adaptation, salinity reaction norms were determined for sets of strains originating from three different salinity regimes of the gradient. Modelled oceanographic connectivity was compared to directional relative migration by correlation analyses to examine oceanographic drivers. Population genetic analyses showed distinct genetic divergence of a low‐salinity Baltic Sea population and a high‐salinity North Sea population, coinciding with the most evident physical dispersal barrier in the area, the Danish Straits. Baltic Sea populations displayed reduced genetic diversity compared to North Sea populations. Growth optima of low salinity isolates were significantly lower than those of strains from higher native salinities, indicating local salinity adaptation. Although the North Sea–Baltic Sea transition was identified as a barrier to gene flow, migration between Baltic Sea and North Sea populations occurred. However, the presence of differentiated neutral markers on each side of the transition zone suggests that migrants are maladapted. It is concluded that local salinity adaptation, supported by oceanographic connectivity patterns creating an asymmetric migration pattern between the Baltic Sea and the North Sea, determines genetic differentiation patterns in the transition zone.     

Proteomics: a link between genomics,genetics and physiology

Thanks to spectacular advances in the techniques for identifying proteins separated by two-dimensional electrophoresis and in methods for large-scale analysis of proteome variations, proteomics is becoming an essential methodology in various fields of plant biology. In the study of pleiotropic effects of mutants and in the analysis of responses to hormones and to environmental changes, the identification of involved metabolic pathways can be deduced from the function of affected proteins. In molecular quantitative genetics, proteomics can be used to map translated genes and loci controlling their expression, which can be used to identify proteins accounting for the variation of complex phenotypic traits. Linking gene expression to cell metabolism on the one hand and to genetic maps on the other, proteomics is a central tool for functional genomics.     

Population genomics meet Lagrangian simulations: Oceanographic patterns and long larval duration ensure connectivity among Paracentrotus lividus populations in the Adriatic and Ionian seas

Connectivity between populations influences both their dynamics and the genetic structuring of species. In this study, we explored connectivity patterns of a marine species with long‐distance dispersal, the edible common sea urchin Paracentrotus lividus, focusing mainly on the Adriatic–Ionian basins (Central Mediterranean). We applied a multidisciplinary approach integrating population genomics, based on 1,122 single nucleotide polymorphisms (SNPs) obtained from 2b‐RAD in 275 samples, with Lagrangian simulations performed with a biophysical model of larval dispersal. We detected genetic homogeneity among eight population samples collected in the focal Adriatic–Ionian area, whereas weak but significant differentiation was found with respect to two samples from the Western Mediterranean (France and Tunisia). This result was not affected by the few putative outlier loci identified in our dataset. Lagrangian simulations found a significant potential for larval exchange among the eight Adriatic–Ionian locations, supporting the hypothesis of connectivity of P. lividus populations in this area. A peculiar pattern emerged from the comparison of our results with those obtained from published P. lividus cytochrome b (cytb) sequences, the latter revealing genetic differentiation in the same geographic area despite a smaller sample size and a lower power to detect differences. The comparison with studies conducted using nuclear markers on other species with similar pelagic larval durations in the same Adriatic–Ionian locations indicates species‐specific differences in genetic connectivity patterns and warns against generalizing single‐species results to the entire community of rocky shore habitats.     

Population genomics of eusocial insects: the costs of a vertebrate‐like effective population size

The evolution of reproductive division of labour and social life in social insects has lead to the emergence of several life‐history traits and adaptations typical of larger organisms: social insect colonies can reach masses of several kilograms, they start reproducing only when they are several years old, and can live for decades. These features and the monopolization of reproduction by only one or few individuals in a colony should affect molecular evolution by reducing the effective population size. We tested this prediction by analysing genome‐wide patterns of coding sequence polymorphism and divergence in eusocial vs. noneusocial insects based on newly generated RNA‐seq data. We report very low amounts of genetic polymorphism and an elevated ratio of nonsynonymous to synonymous changes – a marker of the effective population size – in four distinct species of eusocial insects, which were more similar to vertebrates than to solitary insects regarding molecular evolutionary processes. Moreover, the ratio of nonsynonymous to synonymous substitutions was positively correlated with the level of social complexity across ant species. These results are fully consistent with the hypothesis of a reduced effective population size and an increased genetic load in eusocial insects, indicating that the evolution of social life has important consequences at both the genomic and population levels.     

Making the connection: expanding the role of restoration genetics in restoring and evaluating connectivity

The success of restoration activities is affected by connectivity with the surrounding landscape. From a genetic perspective, landscape connectivity can influence gene flow, effective size, and genetic diversity of populations, which in turn have impacts on the fitness and adaptive potential of species in restored areas. Researchers and practitioners are increasingly using genetic data to incorporate elements of connectivity into restoration planning and evaluation. We show that genetic studies of connectivity can improve restoration planning in three main ways. First, by comparing genetic estimates of contemporary and historical gene flow and population size, practitioners can establish historical baselines that may provide targets for restoration of connectivity. Second, empirical estimates of dispersal, landscape resistance to movement, and adaptive genetic variance can be derived from genetic data and used to parameterize existing restoration planning tools. Finally, restoration actions can also be targeted to remove barriers to gene flow or mitigate pinch‐points in corridors. We also discuss appropriate methods for evaluating the restoration of gene flow over timescales required by practitioners. Collaboration between restoration geneticists, ecologists, and practitioners is needed to develop practical and innovative ways to further incorporate connectivity into restoration practice.     

Seascape genetics of the stalked kelp Pterygophora californica and comparative population genetics in the Santa Barbara Channel

We conducted a population genetic analysis of the stalked kelp, Pterygophora californica, in the Santa Barbara Channel, California, USA. The results were compared with previous work on the genetic differentiation of giant kelp, Macrocystis pyrifera, in the same region. These two sympatric kelps not only share many life history and dispersal characteristics but also differ in that dislodged P. californica does not produce floating rafts with buoyant fertile sporophytes, commonly observed for M. pyrifera. We used a comparative population genetic approach with these two species to test the hypothesis that the ability to produce floating rafts increases the genetic connectivity among kelp patches in the Santa Barbara Channel. We quantified the association of habitat continuity and oceanographic distance with the genetic differentiation observed in stalked kelp, like previously conducted for giant kelp. We compared both overall (across all patches) and pairwise (between patches) genetic differentiation. We found that oceanographic transit time, habitat continuity, and geographic distance were all associated with genetic connectivity in P. californica, supporting similar previous findings for M. pyrifera. Controlling for differences in heterozygosity between kelp species using Jost's D_EST, we showed that global differentiation and pairwise differentiation were similar among patches between the two kelp species, indicating that they have similar dispersal capabilities despite their differences in rafting ability. These results suggest that rafting sporophytes do not play a significant role in effective dispersal of M. pyrifera at ecologically relevant spatial and temporal scales.     

Fine-scale genetic population structure in a mobile marine mammal: inshore bottlenose dolphins in Moreton Bay, Australia

Highly mobile marine species in areas with no obvious geographic barriers are expected to show low levels of genetic differentiation. However, small‐scale variation in habitat may lead to resource polymorphisms and drive local differentiation by adaptive divergence. Using nuclear microsatellite genotyping at 20 loci, and mitochondrial control region sequencing, we investigated fine‐scale population structuring of inshore bottlenose dolphins (Tursiops aduncus) inhabiting a range of habitats in and around Moreton Bay, Australia. Bayesian structure analysis identified two genetic clusters within Moreton Bay, with evidence of admixture between them (F_ST = 0.05, P = 0.001). There was only weak isolation by distance but one cluster of dolphins was more likely to be found in shallow southern areas and the other in the deeper waters of the central northern bay. In further analysis removing admixed individuals, southern dolphins appeared genetically restricted with lower levels of variation (AR = 3.252, π = 0.003) and high mean relatedness (r = 0.239) between individuals. In contrast, northern dolphins were more diverse (AR = 4.850, π = 0.009) and were mixing with a group of dolphins outside the bay (microsatellite‐based STRUCTURE analysis), which appears to have historically been distinct from the bay dolphins (mtDNA Φ_ST = 0.272, P < 0.001). This study demonstrates the ability of genetic techniques to expose fine‐scale patterns of population structure and explore their origins and mechanisms. A complex variety of inter‐related factors including local habitat variation, differential resource use, social behaviour and learning, and anthropogenic disturbances are likely to have played a role in driving fine‐scale population structure among bottlenose dolphins in Moreton Bay.     

Temporal stability and assignment power of adaptively divergent genomic regions between herring (Clupea harengus) seasonal spawning aggregations

Atlantic herring (Clupea harengus), a vital ecosystem component and target of the largest Northwest Atlantic pelagic fishery, undergo seasonal spawning migrations that result in elusive sympatric population structure. Herring spawn mostly in fall or spring, and genomic differentiation was recently detected between these groups. Here we used a subset of this differentiation, 66 single nucleotide polymorphisms (SNPs) to analyze the temporal dynamics of this local adaptation and the applicability of SNP subsets in stock assessment. We showed remarkable temporal stability of genomic differentiation corresponding to spawning season, between samples taken a decade apart (2005 N = 90 vs. 2014 N = 71) in the Gulf of St. Lawrence, and new evidence of limited interbreeding between spawning components. We also examined an understudied and overexploited herring population in Bras d'Or lake (N = 97); using highly reduced SNP panels (N_SNPs > 6), we verified little‐known sympatric spawning populations within this unique inland sea. These results describe consistent local adaptation, arising from asynchronous reproduction in a migratory and dynamic marine species. Our research demonstrates the efficiency and precision of SNP‐based assessments of sympatric subpopulations; and indeed, this temporally stable local adaptation underlines the importance of such fine‐scale management practices.     

Integrative population genetics and metagenomics reveals urbanization increases pathogen loads and decreases connectivity in a wild bee

As urbanization continues to increase, it is expected that two-thirds of the human population will reside in cities by 2050. Urbanization fragments and degrades natural landscapes, threatening wildlife including economically important species such as bees. In this study, we employ whole genome sequencing to characterize the population genetics, metagenome and microbiome, and environmental stressors of a common wild bee, Ceratina calcarata. Population genomic analyses revealed the presence of low genetic diversity and elevated levels of inbreeding. Through analyses of isolation by distance, resistance, and environment across urban landscapes, we found that green spaces including shrubs and scrub were the most optimal pathways for bee dispersal, and conservation efforts should focus on preserving these land traits to maintain high connectivity across sites for wild bees. Metagenomic analyses revealed landscape sites exhibiting urban heat island effects, such as high temperatures and development but low precipitation and green space, had the highest taxa alpha diversity across all domains even when isolating for potential pathogens. Notably, the integration of population and metagenomic data showed that reduced connectivity in urban areas is not only correlated with lower relatedness among individuals but is also associated with increased pathogen diversity, exposing vulnerable urban bees to more pathogens. Overall, our combined population and metagenomic approach found significant environmental variation in bee microbiomes and nutritional resources even in the absence of genetic differentiation, as well as enabled the potential early detection of stressors to bee health.     

Biodiversity,biogeography, and connectivity of polychaetes in the world's largest marine minerals exploration frontier

Aim

The abyssal Clarion-Clipperton Zone (CCZ), Pacific Ocean, is an area of commercial importance owing to the growing interest in mining high-grade polymetallic nodules at the seafloor for battery metals. Research into the spatial patterns of faunal diversity, composition, and population connectivity is needed to better understand the ecological impacts of potential resource extraction. Here, a DNA taxonomy approach is used to investigate regional-scale patterns of taxonomic and phylogenetic alpha and beta diversity, and genetic connectivity, of the dominant macrofaunal group (annelids) across a 6 million km² region of the abyssal seafloor.

Location

The abyssal seafloor (3932–5055 m depth) of the Clarion-Clipperton Zone, equatorial Pacific Ocean.

Methods

We used a combination of new and published barcode data to study 1866 polychaete specimens using molecular species delimitation. Both phylogenetic and taxonomic alpha and beta diversity metrics were used to analyse spatial patterns of biodiversity. Connectivity analyses were based on haplotype distributions for a subset of the studied taxa.

Results

DNA taxonomy identified 291–314 polychaete species from the COI and 16S datasets respectively. Taxonomic and phylogenetic beta diversity between sites were relatively high and mostly explained by lineage turnover. Over half of pairwise comparisons were more phylogenetically distinct than expected based on their taxonomic diversity. Connectivity analyses in abundant, broadly distributed taxa suggest an absence of genetic structuring driven by geographical location.

Main Conclusions

Species diversity in abyssal Pacific polychaetes is high relative to other deep-sea regions. Results suggest that environmental filtering, where the environment selects against certain species, may play a significant role in regulating spatial patterns of biodiversity in the CCZ. A core group of widespread species have diverse haplotypes but are well connected over broad distances. Our data suggest that the high environmental and faunal heterogeneity of the CCZ should be considered in future policy decisions.