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Evolutionary insights derived from comprehensive analyses of DNA barcoding diversity in marine members of the superorder Peracarida (Crustacea: Malacostraca)

Pedro E. Vieira1, 2*, Pedro Soares1, 2, Henrique Queiroga3 and Filipe O. Costa1, 2
  • 1 Centre of Molecular and Environmental Biology, Department of Biology, University of Minho, Portugal
  • 2 Institute of Science and Innovation for Bio-Sustainability, University of Minho, Portugal
  • 3 Centre for Environmental and Marine Studies, Department of Chemistry, University of Aveiro, Portugal

Problem statement Large-scale global initiatives aiming to acquire a comprehensive catalogue of all living species and tackle the different biodiversity knowledge shortfalls (Hortal et al., 2012), have promoted the generation of vast amounts of DNA sequence data. The use of DNA barcodes as a universal system for DNA-based species identification, namely the mitochondrial cytochrome c oxidase gene (COI), has been shown to be successful in species classification and delimitation in several marine groups (Weigand et al., 2019). Furthermore, it has been contributing to improve the detection of potential new species, particularly cryptic species, and it has been used in numerous evolutionary studies (e.g., Vieira et al., 2019). This vast amount of COI data creates an unprecedented opportunity for extensive investigation of core aspects of molecular evolution in whole taxonomic assemblages, such as the Peracarida. Peracarida is a Superorder of the subphylum Crustacea and one of the most diverse and widely distributed groups of crustaceans. In marine coasts, peracaridean species are among the most ecologically important invertebrates, with high relevance in trophic interactions and constituting one of the dominant groups and key components of marine benthic communities (Ruffo, 1998). According to the World Register of Marine Species (WoRMS), it is composed by 12 orders and more than 20 000 described species, a third of the total number of crustacean species. However, they are also among the least known crustaceans, with an estimated two thirds of undiscovered species. Moreover, detailed analyses of evolutionary insights and patterns of molecular variation in marine members of this group are nearly inexistent. Here we conduct a comprehensive investigation of available COI sequence data, in order to gain insights into evolutionary rates and patterns of molecular evolution within Peracarida. Methodology A curated dataset of the world's marine (including brackish waters) peracarids was compiled on Barcode of Life Data Systems (BOLD), including new and previously generated sequences by the research groups authoring the current manuscript. Additionally, representative sequences of all peracaridean species publicly available on BOLD from marine environments across the world on 01/03/2019 were added. Only barcodes with a minimum length of 500 bp, without stop codons, and with indication of sampling location and taxonomic identification were used. Sequence edition and genetic analyses were performed using the software MEGA 7.0 (Kumar et al., 2016), BEAST 2.4.6 (Bouckaert et al., 2014) and the BOLD analyses tools (Ratnasingham & Hebert, 2013). The Barcode Index Number (BIN) system (Ratnasingham & Hebert, 2013) was used as delimitation criterion for assignment of molecular operational taxonomic units (MOTU) across the full dataset. Results Only 6727 of the 40289 publicly available DNA barcodes in BOLD, fulfilled our quality criteria. These barcodes belong to 571 valid morphospecies (274 genera and 109 families) and 812 Barcode Index Numbers (BINs). The orders Amphipoda and Isopoda were represented by the highest number of sequences (83.3% and 15.4% respectively) and the highest number of morphospecies (460 and 98 respectively). Within the order Amphipoda, the families Talitridae and Ampithoidae had the highest number of morphospecies (29 and 28 respectively), while within the order Isopoda, the families Idoteidae (22) and Sphaeromatidae (17) displayed the highest values. The family Hyalidae (order Amphipoda) had the highest proportion of BINs compared to morphospecies (216%). The overall mean intra-specific distance was 1.91% (max. 52.94%), congeneric 23.26% (max. 45.49%) and confamilial 26.20% (max. 59.68%). However, the mean distance among BINs was 18.81%. The family Cressidae (Amphipoda) displayed the highest mean congeneric values (35.68%), while the family Gammarellidae (Amphipoda) the lowest (11.40%). The mean GC content was 38.28% [24.96-50.49%], with the first codon position with the highest values (46.50%), followed by the second (42.54%) and the third (25.79%). The families Pseudidotheidae (Isopoda) and Lycaeidae (Amphipoda) displayed the highest and lowest GC content, respectively (43.85% and 27.49%). Major conclusions COI sequence data suggested an impressive amount of hidden diversity among marine peracarids, adding circa 40% more suspected species in relation to morphospecies. The most notorious taxa contributed disproportionally to the total number of potential new species, surpassing 10 hidden taxa in some cases and contributing with almost 1/3 of additional suspected species. Moreover, just 9 morphospecies contributed with 35% to the this “excess” species. GC content and genetic distances, in particular congeneric, varied considerably among families, suggesting appreciable differences in molecular evolution rates. Some families were considerably phylogenetically divergent from the remaining, which brings insights about taxonomic differences in evolutionary rates within this superorder.

Acknowledgements

This study was supported by the project The NextSea (NORTE-01-0145-FEDER-000032), under the PORTUGAL 2020 Partnership Agreement, through the European Regional Development Fund (ERDF).

References

Bouckaert R et al., 2014. BEAST 2: A software platform for Bayesian evolutionary analysis. PLoS Computational Biology 10(4), e1003537. https://doi.org/10.1371/journal.pcbi.1003537 Hortal J et al., 2015. Seven Shortfalls that Beset Large-Scale Knowledge of Biodiversity. Annual Review of Ecology, Evolution, and Systematics 46:523-549. https://doi.org/10.1146/annurev-ecolsys-112414-054400 Kumar S et al., 2016. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33: 1870-1874. https://10.1093/molbev/msw054 Ratnasingham S & Hebert PDN, 2013. A DNA-based registry for all animal species: the barcode index number (BIN) system. PLoS One 8, e66213. https://doi.org/10.1371/journal.pone.0066213 Ruffo S, 1998. The Amphipoda of the Mediterranean. Memoires de l’institut Oceanographique de Monaco. No. 13. Vieira PE et al., 2019. Deep segregation in the open ocean: Macaronesia as an evolutionary hotspot for low dispersal marine invertebrates. Molecular Ecology 28:1784–1800. https://doi.org/10.1111/mec.15052 Weigand H et al., 2019. DNA barcode reference libraries for the monitoring of aquatic biota in Europe: Gap-analysis and recommendations for future work. Science of The Total Environment 678: 499-524. https://doi.org/10.1016/j.scitotenv.2019.04.247. WoRMS, 2019. Peracarida. Accessed at: http://marinespecies.org/aphia.php?p=taxdetails&id=1090 on 2019-05-02

Keywords: Peracarida, DNA barcoding, meta-species, marine, Molecular variation

Conference: XX Iberian Symposium on Marine Biology Studies (SIEBM XX) , Braga, Portugal, 9 Sep - 12 Sep, 2019.

Presentation Type: Oral Presentation

Topic: Ecology, Biodiversity and Vulnerable Ecosystems

Citation: Vieira PE, Soares P, Queiroga H and Costa FO (2019). Evolutionary insights derived from comprehensive analyses of DNA barcoding diversity in marine members of the superorder Peracarida (Crustacea: Malacostraca). Front. Mar. Sci. Conference Abstract: XX Iberian Symposium on Marine Biology Studies (SIEBM XX) . doi: 10.3389/conf.fmars.2019.08.00058

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Received: 22 May 2019; Published Online: 27 Sep 2019.

* Correspondence: Dr. Pedro E Vieira, Centre of Molecular and Environmental Biology, Department of Biology, University of Minho, Braga, Braga, 4710-057, Portugal, pedroefrvieira@gmail.com