Host population crashes disrupt the diversity of associated marine microbiomes.

Host-associated microbial communities are shaped by myriad factors ranging from host conditions, environmental conditions and other microbes. Disentangling the ecological impact of each of these factors can be particularly difficult as many variables are correlated. Here, we leveraged earthquake-induced changes in host population structure to assess the influence of population crashes on marine microbial ecosystems. A large (7.8 magnitude) earthquake in New Zealand in 2016 led to widespread coastal uplift of up to ~6 m, sufficient to locally extirpate some intertidal southern bull kelp populations. These uplifted populations are slowly recovering, but remain at much lower densities than at nearby, less-uplifted sites. By comparing the microbial communities of the hosts from disturbed and relatively undisturbed populations using 16S rRNA gene amplicon sequencing, we observed that disturbed host populations supported higher functional, taxonomic and phylogenetic microbial beta diversity than non-disturbed host populations. Our findings shed light on microbiome ecological assembly processes, particularly highlighting that large-scale disturbances that affect host populations can dramatically influence microbiome structure. We suggest that disturbance-induced changes in host density limit the dispersal opportunities of microbes, with host community connectivity declining with the density of host populations.

Integrating kelp genomic analyses and geological data to reveal ancient earthquake impacts.

Detached buoyant kelp can disperse thousands of kilometres at sea and can colonize newly available shores in the wake of disturbances that wipe out competitors. Localized earthquake uplift can cause extirpation of intertidal kelp populations followed by recolonization. Sources of recolonizing kelp can be detectable in genomic structure of contemporary populations. Our field observations combined with LiDAR mapping identified a previously unrecognized zone of uplifted rocky coastline in a region that is slowly subsiding. Intertidal kelp (Durvillaea antarctica) on the uplifted section of coast is genetically distinctive from nearby populations, with genomic signatures most similar to that of kelp 300 km to the south. Genetic divergence between these locations suggests reproductive isolation for thousands of years. Combined geological and genetic data suggest that this uplift event occurred during one of four major earthquakes between 6000 and 2000 years ago, with one of the younger events most likely. Extirpation of the pre-existing kelp required sudden uplift of approximately 2 metres, precluding several small incremental uplift events. Our results show the power of integrating biological (genomic) analyses with geological data to understand ancient geological processes and their ecological impacts.

Parallel recolonizations generate distinct genomic sectors in kelp following high-magnitude earthquake disturbance.

Large-scale disturbance events have the potential to drastically reshape biodiversity patterns. Notably, newly vacant habitat space cleared by disturbance can be colonized by multiple lineages, which can lead to the evolution of distinct spatial "sectors" of genetic diversity within a species. We test for disturbance-driven sectoring of genetic diversity in intertidal southern bull kelp, Durvillaea antarctica (Chamisso) Hariot, following the high-magnitude 1855 Wairarapa earthquake in New Zealand. Specifically, we use genotyping-by-sequencing (GBS) to analyse fine-scale population structure across the uplift zone and apply machine learning to assess the fit of alternative recolonizaton models. Our analysis reveals that specimens from the uplift zone carry distinctive genomic signatures potentially linked to post-earthquake recolonization processes. Specifically, our analysis identifies two parapatric spatial-genomic sectors of D. antarctica at Turakirae Head, which experienced the most dramatic uplift. Based on phylogeographical modelling, we infer that bull kelp in the Wellington region was probably a source for recolonization of the heavily uplifted Turakirae Head coastline, via two parallel, eastward recolonization events. By identifying multiple parapatric genotypic sectors within a recently recolonized coastal region, the current study provides support for the hypothesis that competing lineage expansions can generate striking spatial structuring of genetic diversity, even in highly dispersive taxa.

Lurking in the water: testing eDNA metabarcoding as a tool for ecosystem-wide parasite detection.

In the light of global biodiversity change and emerging disease, there is an urgent need to establish efficient monitoring programmes of parasites in aquatic ecosystems. However, parasite identification is time-consuming, requires a high degree of taxonomic expertize and in general requires lethal sampling. The use of environmental DNA methodology to identify parasites has the potential to circumvent these limitations. This study evaluates the use of eDNA metabarcoding to detect the presence of all species of nematode and platyhelminth parasites in two New Zealand lakes. We developed two novel metabarcoding primer pairs targeting a region of cytochrome oxidase I gene (COI) specific to platyhelminths and nematodes. We successfully detected parasite DNA in both lakes. Platyhelminth DNA yield was in general greater than nematode DNA yield. This most likely results from the larger biomass of the former quantified using traditional methods, or the presence of free-swimming life stages in the life cycle of many platyhelminths. By using eDNA, we did not detect all expected parasite families revealed through traditional methods, likely due to a lack of sequencing data available from public databases such as GenBank. As such, genetic resources need to include full reference sequences if parasitology is to truly harness eDNA to characterize and monitor parasite biodiversity in natural systems.

A duplicated amh is the master sex-determining gene for Sebastes rockfish in the Northwest Pacific.

Teleost fish are the most diverse group of vertebrates and provide opportunities to study the evolution of sex determination (SD) systems. Using genomic and functional analyses, we identified a male-specific duplication of anti-Müllerian hormone (amh) gene as the male master sex-determining (MSD) gene in Sebastes schlegelii. By resequencing 10 males and 10 females, we characterized a 5 kb-long fragment in HiC_Scaffold_12 as a male-specific region, which contained an amh gene (named amhy). We then demonstrated that amhy is a duplication of autosomal amh that was later translocated to the ancestral Y chromosome. amha and amhy shared high-nucleotide identity with the most significant difference being two insertions in intron 4 of amhy. Furthermore, amhy overexpression triggered female-to-male sex reversal in S. schlegelii, displaying its fundamental role in driving testis differentiation. We developed a PCR assay which successfully identified sexes in two species of northwest Pacific rockfish related to S. schlegelii. However, the PCR assay failed to distinguish the sexes in a separate clade of northeast Pacific rockfish. Our study provides new examples of amh as the MSD in fish and sheds light on the convergent evolution of amh duplication as the driving force of sex determination in different fish taxa.

Adaptive markers distinguish North and South Pacific Albacore amid low population differentiation.

Albacore (Thunnus alalunga) support an economically valuable global fishery, but surprisingly little is known about the population structure of this highly migratory species. Physical tagging data suggest that Albacore from the North and South Pacific Ocean are separate stocks, but results from previous genetic studies did not support this two stock hypothesis. In addition, observed biological differences among juveniles suggest that there may be population substructure in the North Pacific. We used double-digest restriction site-associated DNA sequencing to assess population structure among 308 Albacore caught in 12 sample areas across the Pacific Ocean (10 North, 2 South). Since Albacore are highly migratory and spawning areas are unknown, sample groups were not assumed to be equivalent to populations and the genetic data were analyzed iteratively. We tested for putatively adaptive differences among groups and for genetic variation associated with sex. Results indicated that Albacore in the North and South Pacific can be distinguished using 84 putatively adaptive loci, but not using the remaining 12,788 presumed neutral sites. However, two individuals likely represent F1 hybrids between the North and South Pacific populations, and 43 Albacore potentially exhibit lower degrees of mixed ancestry. In addition, four or five cross-hemisphere migrants were potentially identified. No genetic evidence was found for population substructure within the North Pacific, and no loci appeared to distinguish males from females. Potential functions for the putatively adaptive loci were identified, but an annotated Albacore genome is required for further exploration. Future research should try to locate spawning areas so that life history, demography, and genetic population structure can be linked and spatiotemporal patterns can be investigated.

Northward range extension for Durvillaea poha bull kelp: Response to tectonic disturbance?

Understanding the forces that shape species distributions is increasingly important in a fast-changing world. Although major disturbance events can adversely affect natural populations, they can also present new opportunities, for example by opening up habitat for colonization by other lineages. Following extensive geographic sampling, we use genomic data to infer a range extension following disturbance for an ecologically important intertidal macroalgal species. Specifically, we genotyped 288 southern bull kelp (Durvillaea) plants from 28 localities across central New Zealand. All specimens from the North Island were expected to be D. antarctica, but unexpectedly 10 samples from four sites were identified as D. poha. Extensive sampling from the northern South Island (105 samples at five locations) confirmed the absence of D. poha north of the Kaikoura Peninsula. The North Island specimens of D. poha therefore reveal a biogeographic disjunction, some 150 km northeast of the nearest (South Island) population of this species. Based on strong geographic correspondence between these North Island samples and historic disturbance, we infer that tectonic upheaval, particularly earthquake-generated landslides, likely extirpated local D. antarctica and created an opportunity for a northward range expansion event by D. poha. Close phylogenomic relationships between this new North Island population and South Island samples support a geologically recent northward expansion, rather than a deeper evolutionary origin. These findings indicate the potential of large-scale disturbances to facilitate sudden biogeographic range expansions, and they emphasize the ability of genomic analyses with fine-scale sampling to reveal long-lasting signatures of past disturbance, dispersal, and colonization.

Lineage Identification Affects Estimates of Evolutionary Mode in Marine Snails.

In order to study evolutionary pattern and process, we need to be able to accurately identify species and the evolutionary lineages from which they are derived. Determining the concordance between genetic and morphological variation of living populations, and then directly comparing extant and fossil morphological data, provides a robust approach for improving our identification of lineages through time. We investigate genetic and shell morphological variation in extant species of Penion marine snails from New Zealand, and extend this analysis into deep time using fossils. We find that genetic and morphological variation identify similar patterns and support most currently recognized extant species. However, some taxonomic over-splitting is detected due to shell size being a poor trait for species delimitation, and we identify incorrect assignment of some fossil specimens. We infer that a single evolutionary lineage (Penion sulcatus) has existed for 22 myr, with most aspects of shell shape and shell size evolving under a random walk. However, by removing samples previously classified as the extinct species P. marwicki, we instead detect morphological stasis for one axis of shell shape variation. This result demonstrates how lineage identification can change our perception of evolutionary pattern and process. [Genotyping by sequencing; geometric morphometrics; morphological evolution; Neogastropoda; phenotype; speciation; stasis.].

Sex matters: Otolith shape and genomic variation in deacon rockfish (Sebastes diaconus).

Little is known about intraspecific variation within the deacon rockfish (Sebastes diaconus), a recently described species found in the northeast Pacific Ocean. We investigated population structure among fish sampled from two nearshore reefs (Siletz Reef and Seal Rock) and one offshore site (Stonewall Bank) within a <50-km2 area off the Oregon coast. Fish from the three sample sites exhibited small but statistically significant differences based on genetic variation at >15,000 neutral loci, whether analyzed independently or classified into nearshore and offshore groups. Male and females were readily distinguished using genetic data and 92 outlier loci were associated with sex, potentially indicating differential selection between males and females. Morphometric results indicated that there was significant secondary sexual dimorphism in otolith shape, but further sampling is required to disentangle potential confounding influence of age. This study is the first step toward understanding intraspecific variation within the deacon rockfish and the potential management implications. Since differentiation among the three sample sites was small, we consider the results to be suggestive of a single stock. However, future studies should evaluate how the stock is affected by differences in sex, age, and gene flow between the nearshore and offshore environments.

Characterizing neutral and adaptive genomic differentiation in a changing climate: The most northerly freshwater fish as a model.

Arctic freshwater ecosystems have been profoundly affected by climate change. Given that the Arctic charr (Salvelinus alpinus) is often the only fish species inhabiting these ecosystems, it represents a valuable model for studying the impacts of climate change on species life-history diversity and adaptability. Using a genotyping-by-sequencing approach, we identified 5,976 neutral single nucleotide polymorphisms and found evidence for reduced gene flow between allopatric morphs from two high Arctic lakes, Linne'vatn (Anadromous, Normal, and Dwarf) and Ellasjøen (Littoral and Pelagic). Within each lake, the degree of genetic differentiation ranged from low (Pelagic vs. Littoral) to moderate (Anadromous and Normal vs. Dwarf). We identified 17 highly diagnostic, putatively adaptive SNPs that differentiated the allopatric morphs. Although we found no evidence for adaptive differences between morphs within Ellasjøen, we found evidence for moderate (Anadromous vs. Normal) to high genetic differentiation (Anadromous and Normal vs. Dwarf) among morphs within Linne'vatn based on two adaptive loci. As these freshwater ecosystems become more productive, the frequency of sympatric morphs in Ellasjøen will likely shift based on foraging opportunities, whereas the propensity to migrate may decrease in Linne'vatn, increasing the frequency of the Normal morph. The Dwarf charr was the most genetically distinct group. Identifying the biological basis for small body size should elucidate the potential for increased growth and subsequent interbreeding with sympatric morphs. Overall, neutral and adaptive genomic differentiation between allopatric and some sympatric morphs suggests that the response of Arctic charr to climate change will be variable across freshwater ecosystems.

Evolutionary lineages of marine snails identified using molecular phylogenetics and geometric morphometric analysis of shells.

The relationship between morphology and inheritance is of perennial interest in evolutionary biology and palaeontology. Using three marine snail genera Penion, Antarctoneptunea and Kelletia, we investigate whether systematics based on shell morphology accurately reflect evolutionary lineages indicated by molecular phylogenetics. Members of these gastropod genera have been a taxonomic challenge due to substantial variation in shell morphology, conservative radular and soft tissue morphology, few known ecological differences, and geographical overlap between numerous species. Sampling all sixteen putative taxa identified across the three genera, we infer mitochondrial and nuclear ribosomal DNA phylogenetic relationships within the group, and compare this to variation in adult shell shape and size. Results of phylogenetic analysis indicate that each genus is monophyletic, although the status of some phylogenetically derived and likely more recently evolved taxa within Penion is uncertain. The recently described species P. lineatus is supported by genetic evidence. Morphology, captured using geometric morphometric analysis, distinguishes the genera and matches the molecular phylogeny, although using the same dataset, species and phylogenetic subclades are not identified with high accuracy. Overall, despite abundant variation, we find that shell morphology accurately reflects genus-level classification and the corresponding deep phylogenetic splits identified in this group of marine snails.

Genome statistics and phylogenetic reconstructions for Southern Hemisphere whelks (Gastropoda: Buccinulidae).

This data article provides genome statistics, phylogenetic networks and trees for a phylogenetic study of Southern Hemisphere Buccinulidae marine snails [1]. We present alternative phylogenetic reconstructions using mitochondrial genomic and 45S nuclear ribosomal cassette DNA sequence data, as well as trees based on short-length DNA sequence data. We also investigate the proportion of variable sites per sequence length for a set of mitochondrial and nuclear ribosomal genes, in order to examine the phylogenetic information provided by different DNA markers. Sequence alignment files used for phylogenetic reconstructions in the main text and this article are provided here.

A phylogeny of Southern Hemisphere whelks (Gastropoda: Buccinulidae) and concordance with the fossil record.

Under current marine snail taxonomy, the majority of whelks from the Southern Hemisphere (Buccinulidae) are hypothesised to represent a monophyletic clade that has evolved independently from Northern Hemisphere taxa (Buccinidae). Phylogenetic analysis of mitochondrial genomic and nuclear ribosomal DNA sequence data indicates that Southern Hemisphere taxa are not monophyletic, and results suggest that dispersal across the equator has occurred in both directions. New Zealand buccinulid whelks, noted for their high endemic diversity, are also found to not be monophyletic. Using independent fossil calibrations, estimated genetic divergence dates show remarkable concordance with the fossil record of the Penion and Kelletia. The divergence dates and the geographic distribution of the genera through time implies that some benthic marine snails are capable of dispersal over long distances, despite varied developmental strategies. Phylogenetic results also indicate that one species, P. benthicolus belongs in Antarctoneptunea.