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Abstract. Mitochondrial genomes can be assembled readily from shotgun sequenced DNA mixtures of mass-trapped arthropods ('mitochondrial metagenomics'), speeding up the taxonomic characterization. Bulk sequencing was conducted on some 800 individuals of Diptera obtained by canopy-fogging of a single tree in Borneo dominated by small (<1.5 mm) individuals. Specimens were split into five body-size classes for DNA extraction, to equalize read numbers across specimens and to study how body size, a key ecological trait, interacts with species and phylogenetic diversity. Genome assembly produced 304 orthologous Accepted ArticleThis article is protected by copyright. All rights reserved.mitochondrial contigs presumed to each represent a different species. The small-bodied fraction was the by far most species-rich (187 contigs). Identification of contigs was through phylogenetic analysis together with 56 reference mitogenomes, which placed most of the Bornean community into seven clades of small-bodied species, indicating phylogenetic conservation of body size. Mapping of shotgun reads against the mitogenomes showed wide ranges of read abundances within each size class. Ranked read-abundance plots were largely log-linear, indicating a uniformly filled abundance spectrum, especially for smallbodied species. Small-bodied species differed greatly from other size classes in neutral metacommunity parameters, exhibiting greater levels of immigration, besides greater total community size. We suggest that the established uses of mitochondrial metagenomics for analysis of species and phylogenetic diversity can be extended to parameterise recent theories of community ecology and biodiversity, and by focusing on the number mitochondria, rather than individuals, a new theoretical framework for analysis of mitochondrial abundance spectra can be developed that incorporates metabolic activity approximated by the count of mitochondria.
Background: Pteropods are planktonic gastropods that are considered as bio-indicators to monitor impacts of ocean acidification on marine ecosystems. In order to gain insight into their adaptive potential to future environmental changes, it is critical to use adequate molecular tools to delimit species and population boundaries and to assess their genetic connectivity. We developed a set of target capture probes to investigate genetic variation across their large-sized genome using a population genomics approach. Target capture is less limited by DNA amount and quality than other genome-reduced representation protocols, and has the potential for application on closely related species based on probes designed from one species. Results: We generated the first draft genome of a pteropod, Limacina bulimoides, resulting in a fragmented assembly of 2.9 Gbp. Using this assembly and a transcriptome as a reference, we designed a set of 2899 genomewide target capture probes for L. bulimoides. The set of probes includes 2812 single copy nuclear targets, the 28S rDNA sequence, ten mitochondrial genes, 35 candidate biomineralisation genes, and 41 non-coding regions. The capture reaction performed with these probes was highly efficient with 97% of the targets recovered on the focal species. A total of 137,938 single nucleotide polymorphism markers were obtained from the captured sequences across a test panel of nine individuals. The probes set was also tested on four related species: L. trochiformis, L. lesueurii, L. helicina, and Heliconoides inflatus, showing an exponential decrease in capture efficiency with increased genetic distance from the focal species. Sixty-two targets were sufficiently conserved to be recovered consistently across all five species. Conclusion: The target capture protocol used in this study was effective in capturing genome-wide variation in the focal species L. bulimoides, suitable for population genomic analyses, while providing insights into conserved genomic regions in related species. The present study provides new genomic resources for pteropods and supports the use of target capture-based protocols to efficiently characterise genomic variation in small non-model organisms with large genomes.
Background The aragonite shelled, planktonic gastropod family Atlantidae (shelled heteropods) is likely to be one of the first groups to be impacted by imminent ocean changes, including ocean warming and ocean acidification. With a fossil record spanning at least 100 Ma, atlantids have experienced and survived global-scale ocean changes and extinction events in the past. However, the diversification patterns and tempo of evolution in this family are largely unknown. Results Based on a concatenated maximum likelihood phylogeny of three genes (cytochrome c oxidase subunit 1 mitochondrial DNA, 28S and 18S ribosomal rRNA) we show that the three extant genera of the family Atlantidae, Atlanta, Protatlanta and Oxygyrus, form monophyletic groups. The genus Atlanta is split into two groups, one exhibiting smaller, well ornamented shells, and the other having larger, less ornamented shells. The fossil record, in combination with a fossil-calibrated phylogeny, suggests that large scale atlantid extinction was accompanied by considerable and rapid diversification over the last 25 Ma, potentially driven by vicariance events. Conclusions Now confronted with a rapidly changing modern ocean, the ability of atlantids to survive past global change crises gives some optimism that they may be able to persist through the Anthropocene.
Little is known about when and how planktonic species arise and persist in the open ocean without apparent dispersal barriers. Pteropods are planktonic snails with thin shells susceptible to dissolution that are used as bio‐indicators of ocean acidification. However, distinct evolutionary units respond to acidification differently, and defining species boundaries is therefore crucial for predicting the impact of changing ocean conditions. In this global population genomic study of the shelled pteropod Limacina bulimoides, we combined genetic (759,000 single nucleotide polymorphisms) and morphometric data from 161 individuals, revealing three major genetic lineages (FST = 0.29–0.41): an “Atlantic lineage” sampled across the Atlantic, an “Indo‐Pacific lineage” sampled in the North Pacific and Indian Ocean, and a “Pacific lineage” sampled in the North and South Pacific. A time‐calibrated phylogeny suggests that the lineages diverged about 1 million years ago, with estimated effective population size remaining high (~10 million) throughout Pleistocene glacial cycles. We do not observe any signatures of recent hybridization, even in areas of sympatry in the North Pacific. While the lineages are reproductively isolated, they are morphologically cryptic, with overlapping shell shape and shell colour distributions. Despite showing that the circumglobal L. bulimoides consists of multiple species with smaller ranges than initially thought, we found that these pteropods still possess high levels of genetic variability. Our study adds to the growing evidence that speciation is often overlooked in the open ocean, and suggests the presence of distinct biological species within many other currently defined circumglobal planktonic species.
PCR-free techniques such as meta-mitogenomics (MMG) can recover taxonomic composition of macroinvertebrate communities, but suffer from low efficiency, as >90% of sequencing data is mostly uninformative due to the great abundance of nuclear DNA that cannot be identified with current reference databases. Current MMG studies do not routinely check data for information on macroinvertebrate-associated bacteria and gene functions. However, this could greatly increase the efficiency of MMG studies by revealing yet overlooked diversity within ecosystems and making currently unused data available for ecological studies. By analysing six ‘mock’ communities, each containing three macroinvertebrate taxa, we tested whether this additional data on bacterial taxa and functional potential of communities can be extracted from MMG datasets. Further, we tested whether differential centrifugation, which is known to greatly increase efficiency of macroinvertebrate MMG studies by enriching for mitochondria, impacts on the inferred bacterial community composition. Our results show that macroinvertebrate MMG datasets contain a high number of mostly endosymbiont bacterial taxa and associated gene functions. Centrifugation reduced both the absolute and relative abundance of highly abundant Gammaproteobacteria, thereby facilitating detection of rare taxa and functions. When analysing both taxa and gene functions, the number of features obtained from the MMG dataset increased 31-fold (‘enriched’) respectively 234-fold (‘not enriched’). We conclude that analysing MMG datasets for bacteria and gene functions greatly increases the amount of information available and facilitates the use of shotgun metagenomic techniques for future studies on biodiversity.
The aragonite shelled, planktonic gastropod family Atlantidae (shelled heteropods) is likely to be one of the first groups to be impacted by imminent ocean changes, including ocean warming and ocean acidification. With a fossil record spanning at least 100 Million years (Ma), atlantids have experienced and survived global-scale ocean changes and extinction events in the past. However, the diversification patterns and tempo of evolution in this family are largely unknown. Based on a concatenated maximum likelihood phylogeny of three genes (cytochrome c oxidase subunit 1 mitochondrial DNA, 28S and 18S ribosomal rRNA) we show that the three extant genera of the family Atlantidae, Atlanta, Protatlanta and Oxygyrus, form monophyletic clades. The genus Atlanta is split into two groups, one exhibiting smaller, well ornamented shells, and the other having larger, less ornamented shells. The fossil record, in combination with a fossil-calibrated phylogeny suggest that large scale atlantid extinction was accompanied by considerable and rapid diversification over the last 25 Ma, potentially driven by vicariance events. Now confronted with a rapidly changing modern ocean, the ability of atlantids to survive past global change crises gives some optimism that they may be able to persist through the Anthropocene.
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