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.     

Polygenic evolution drives species divergence and climate adaptation in corals

Closely related species often show substantial differences in ecological traits that allow them to occupy different environmental niches. For few of these systems is it clear what the genomic basis of adaptation is and whether a few loci of major effect or many genome‐wide differences drive species divergence. Four cryptic species of the tabletop coral Acropora hyacinthus are broadly sympatric in American Samoa; here we show that two common species have differences in key environmental traits such as microhabitat distributions and thermal stress tolerance. We compared gene expression patterns and genetic polymorphism between these two species using RNA‐Seq. The vast majority of polymorphisms are shared between species, but the two species show widespread differences in allele frequencies and gene expression, and tend to host different symbiont types. We find that changes in gene expression are related to changes in the frequencies of many gene regulatory variants, but that many of these differences are consistent with the action of genetic drift. However, we observe greater genetic divergence between species in amino acid replacement polymorphisms compared to synonymous variants. These findings suggest that polygenic evolution plays a major role in driving species differences in ecology and resilience to climate change.     

Incorporating climate change adaptation into marine protected area planning

Climate change is increasingly impacting marine protected areas (MPAs) and MPA networks, yet adaptation strategies are rarely incorporated into MPA design and management plans according to the primary scientific literature. Here we review the state of knowledge for adapting existing and future MPAs to climate change and synthesize case studies (n = 27) of how marine conservation planning can respond to shifting environmental conditions. First, we derive a generalized conservation planning framework based on five published frameworks that incorporate climate change adaptation to inform MPA design. We then summarize examples from the scientific literature to assess how conservation goals were defined, vulnerability assessments performed and adaptation strategies incorporated into the design and management of existing or new MPAs. Our analysis revealed that 82% of real‐world examples of climate change adaptation in MPA planning derive from tropical reefs, highlighting the need for research in other ecosystems and habitat types. We found contrasting recommendations for adaptation strategies at the planning stage, either focusing only on climate refugia, or aiming for representative protection of areas encompassing the full range of expected climate change impacts. Recommendations for MPA management were more unified and focused on adaptative management approaches. Lastly, we evaluate common barriers to adopting climate change adaptation strategies based on reviewing studies which conducted interviews with MPA managers and other conservation practitioners. This highlights a lack of scientific studies evaluating different adaptation strategies and shortcomings in current governance structures as two major barriers, and we discuss how these could be overcome. Our review provides a comprehensive synthesis of planning frameworks, case studies, adaptation strategies and management actions which can inform a more coordinated global effort to adapt existing and future MPA networks to continued climate change.     

Development of microsatellite loci in pinto abalone (Haliotis kamtschatkana)

Twelve novel di‐, tri‐ and tetranucleotide microsatellite loci to the pinto abalone (Haliotis kamtschatkana) are described. Over 400 individuals were analysed at each microsatellite locus. Observed heterozygosities ranged from 0.44 to 0.93, and numbers of alleles from 20 to 63. Six of the loci contained excesses in homozygosity indicative of inbreeding, nonrandom mating, population admixture, or null alleles.     

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.     

Perlinhibin, a cysteine-, histidine-, and arginine-rich miniprotein from abalone (Haliotis laevigata) nacre, inhibits in vitro calcium carbonate crystallization

We have isolated a 4.785 Da protein from the nacreous layer of the sea snail Haliotis laevigata (greenlip abalone) shell after demineralization with acetic acid. The sequence of 41 amino acids was determined by Edman degradation supported by mass spectrometry. The most abundant amino acids were cysteine (19.5%), histidine (17%), and arginine (14.6%). The positively charged amino acids were almost counterbalanced by negatively charged ones resulting in a calculated isoelectric point of 7.86. Atomic-force microscopy studies of the interaction of the protein with calcite surfaces in supersaturated calcium carbonate solution or calcium chloride solution showed that the protein bound specifically to calcite steps, inhibiting further crystal growth at these sites in carbonate solution and preventing crystal dissolution when carbonate was substituted with chloride. Therefore this protein was named perlinhibin. X-ray diffraction investigation of the crystal after atomic-force microscopy growth experiments showed that the formation of aragonite was induced on the calcite substrate around holes caused by perlinhibin crystal-growth inhibition. The strong interaction of the protein with calcium carbonate was also shown by vapor diffusion crystallization. In the presence of the protein, the crystal surfaces were covered with holes due to protein binding and local inhibition of crystal growth. In addition to perlinhibin, we isolated and sequenced a perlinhibin-related protein, indicating that perlinhibin may be a member of a family of closely related proteins.     

Perlustrin, a Haliotis laevigata (abalone) nacre protein, is homologous to the insulin-like growth factor binding protein N-terminal module of vertebrates.

The 84-amino-acid-long sequence of perlustrin showed homology of the abalone nacre protein to the N-terminal domain of mammalian insulin-like growth factor binding proteins (IGFBPs). Despite the evolutionary distance between mollusks and mammals, the sequence identity was 40% including 12 conserved cysteines. However, the residues which were suggested recently to bind IGF-II in a complex with IGFBP-5 were conserved only partially. Nevertheless, perlustrin bound human IGFs with K(D) approximately 10(-7) M. This was the same affinity range as measured before for the interaction of isolated IGFBP-5 N-terminal domains with IGFs. Moreover, perlustrin bound bovine insulin with only approximately two- to sevenfold lower affinity than IGFs. Sequence similarity and growth factor binding identified perlustrin unequivocally as a member of the IGFBP family, the first found in an invertebrate biomineral. Nacre is known to contain proteinaceous factors which promote bone formation in vitro and in vivo. Bone contains IGFBPs which influence bone metabolism in many ways by modulating either IGF effects or IGF independently. Thus, perlustrin may provide a first clue at the molecular level to what these two phylogenetically rather distant biomineralization systems have in common.     

Isolation and cross-amplification of microsatellites in pink abalone (Haliotis corrugata)

Ten novel microsatellite loci were isolated in pink abalone, Haliotis corrugata, using (GT)₁₅ and (CT)₁₅ enriched genomic libraries. Two previously reported Haliotis kamtschatkana microsatellites cross‐amplified in H. corrugata. A set of 12 polymorphic microsatellites were evaluated in a wild population sample (N = 49). The number of alleles ranged from two to 55, and the observed and expected heterozygosities ranged from 0.104 to 0.939 and from 0.213 to 0.982, respectively. Significant deviations from Hardy–Weinberg equilibrium at three loci and no linkage disequilibrium were observed. Haliotis corrugata microsatellites cross‐amplified in other abalone species, two in H. fulgens, and seven in H. rufescens.     

Possible range extension in the endangered and understudied winghead shark (Eusphyra blochii)

Here the authors report on a possible range extension in the rare and understudied winghead shark (Eusphyra blochii). A specimen was captured by recreational fishermen in Moreton Bay, Queensland, Australia, c. 800 km south of its current distribution. As winghead sharks show a clumped distribution in Australia associated with river outflow, Moreton Bay, with its large catchment area, may represent a suitable habitat for the species and previous occurrence may have gone undetected. Alternatively, climate change may have caused a recent southward shift in winghead sharks, as observed in other elasmobranch species along Australia's East Coast.     

Isolation and characterization of microsatellite markers in the South African abalone (Haliotis midae)

We report the isolation and characterization of 11 polymorphic microsatellite loci in the South African abalone Haliotis midae. These loci showed a range of five to 21 alleles per locus and observed heterozygosities ranging from 0.14 to 0.93 in a wild population of 32 individuals. All loci except four conformed to Hardy–Weinberg expectations and did not show linkage disequilibrium. The polymorphism exhibited at these loci indicate that they would be useful in determining levels of genetic variability in natural and commercial Haliotis midae populations as well as in parentage and Quantitative Trait Loci (QTL) analysis in hatchery reared abalone.     

Development of 11 polymorphic microsatellite loci in the small abalone (Haliotis diversicolor Reeve)

Eleven polymorphic microsatellite loci for Haliotis diversicolor were isolated and characterized from (CT)(n) - and (AC)(n) -enriched library. They were tested in 24 individuals from a natural population. All of them were polymorphic, with the number of alleles varying between three and 10. The observed heterozygosities and expected heterozygosities ranged from 0.083 to 0.913 and from 0.159 to 0.856, respectively. The 11 isolated microsatellite loci, except SA-JMU6 and SA-JMU12, followed Hardy-Weinberg expectations. Seven sets of primers also amplify in closely related species, H. ovina and H. asinine. These 11 polymorphic microsatellites will be useful for analysing the population structure and genetic diversity in H. diversicolor.     

Species identification of the tropical abalone (Haliotis asinina, Haliotis ovina, and Haliotis varia) in Thailand using RAPD and SCAR markers

A randomly amplified polymorphic DNA (RAPD) analysis was used to identify the species- and population-specific markers of abalone; Haliotis asinina, H. ovina, and H. varia in Thai waters. Fifteen species-specific and six population-specific RAPD markers were identified. In addition, an 1650 bp band (UBC195) that was restricted to H. ovina from the Gulf of Thailand (east) was also found. All of the specific RAPD markers were cloned and sequenced. Twenty pairs of primers were designed and specificity-tested (N = 12 and 4 for target and non-target species, respectively). Seven primer pairs (CUHA1, 2, 4, 11, 12, 13, and 14) were specifically amplified by H. asinina DNA, whereas a single pair of primers showed specificity with H. ovina (CUHO3) and H. varia (CUHV1), respectively. Four primer pairs, including CUHA2, CUHA12, CUHO3, and CUHV1, were further examined against 216 individuals of abalone (N = 111, 73, and 32, respectively). Results indicated the species-specific nature of all of them, except CUHO3, with the sensitivity of detection of 100 pg and 20 pg of the target DNA template for CUHA2 and CUHA12 and CUHV1, respectively. The species-origin of the frozen, ethanol-preserved, dried, and boiled H. asinina specimens could also be successfully identified by CUHA2.     

The amino-acid sequence of the abalone (Haliotis laevigata) nacre protein perlucin. Detection of a functional C-type lectin domain with galactose/mannose specificity.

Perlucin isolated from abalone nacre consists of 155 amino acids including a glycosylated asparagine. The sequence of the first 130 amino acids shows a high similarity to the C-type carbohydrate-recognition domains of asialoglycoprotein receptors and other members of the group of C-type lectins but also a weaker similarity to related proteins without carbohydrate-binding activity. This C-type module is followed by a short C-terminal domain containing two almost identical sequence repeats with a length of 10 amino acids. Solid phase assays show a divalent metal ion-dependent binding of perlucin to (neo)glycoproteins containing D-galactose or D-mannose/D-glucose indicating that perlucin is a functional C-type lectin with broad carbohydrate-binding specificity. Our results also indicate that it may be difficult to predict carbohydrate-binding specificity and the occurrence of alternative binding configurations by amino-acid sequence comparisons and homology modeling.     

'Back to the future': how archaeological remains can describe salmon adaptation to climate change

A strategy for species to survive climate change will be to change adaptively their way of life. Understanding rapid adaptation to climate change is therefore a priority for current research. In this issue, Turrero et al. (2012) use an original approach to unravel life history trait responses to climate change in two fish species (Salmo trutta and S. salar). Going against the flow, the authors adopt the strategy of going back to the future by investigating the responses of fish to the warming periods that followed the Last Glacial Period (approximately 30-20,000 years BP). To do this, they analysed Salmo vertebrae from well-dated archaeological sites in northern Spain in order to uncover key life history traits, which they then compared to those of contemporary specimens. They found that, as the climate got warmer, Salmo species tended to reduce the time spent in growing areas and reached spawning areas at a younger age; this tendency began approximately 15,000 years BP and accelerated in contemporary periods. The implication is a lower age at maturity and a lower reproductive success, which they tentatively related to recent declines in population growth rate. This innovative study demonstrates how changes in life history traits are linked both to the population growth rate and to the evolutionary rate under climatic constraints, which may serve as a basis for future conservation research.     

Using past and present habitat to predict the current distribution and abundance of a rare cryptic lizard,Delma impar (Pygopodidae)

We present logistic regression models predicting the distribution and abundance of a threatened cryptic lizard, Delma impar (Pygopodidae), in the Australian Capital Territory (ACT). The models incorporate current habitat and historical land use and habitat change (woodland clearance, ploughing, grazing, fertilizer application). Information on historical land use was acquired from land survey maps, aerial photographs and from floristic indices of land management. Floristic indices were developed from a survey of local agronomists who scored individual plant species, responses to grazing, ploughing and fertilizer application. Floristic indicies proved to be more informative than floristic ordination analyses. It emerged that historical factors were of key importance for predicting the distribution and abundance of D. impar. Since European settlement, D. impar has apparently spread from primary (naturally treeless grasslands) into secondary grasslands (grassland formerly with an overstorey of trees) and has been locally excluded by some farming activities such as ploughing. We conclude that a combination of current habitat and past changes in habitat may be necessary to understand the current distributions of plant and animal species that have limited dispersal ability and that are susceptible to local temporary habitat destruction. Active conservation strategies involving, for example, assisted dispersal, may be important for these species.