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Delimiting Cryptic Species Within the Brown-Banded Bamboo Shark

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Delimiting Cryptic Species Within the Brown-Banded Bamboo Shark Fahmi et al. BMC Ecol Evo (2021) 21:121 BMC Ecology and Evolution https://doi.org/10.1186/s12862-021-01852-3 RESEARCH ARTICLE Open Access Delimiting cryptic species within the brown-banded bamboo shark, Chiloscyllium punctatum in the Indo-Australian region with mitochondrial DNA and genome-wide SNP approaches Fahmi1,3* , Ian R. Tibbetts1, Michael B. Bennett2 and Christine L. Dudgeon2 Abstract Background: Delimiting cryptic species in elasmobranchs is a major challenge in modern taxonomy due the lack of available phenotypic features. Employing stand-alone genetics in splitting a cryptic species may prove problematic for further studies and for implementing conservation management. In this study, we examined mitochondrial DNA and genome-wide nuclear single nucleotide polymorphisms (SNPs) in the brown-banded bambooshark, Chiloscyllium punctatum to evaluate potential cryptic species and the species-population boundary in the group. Results: Both mtDNA and SNP analyses showed potential delimitation within C. punctatum from the Indo-Australian region and consisted of four operational taxonomic units (OTUs), i.e. those from Indo-Malay region, the west coast of Sumatra, Lesser Sunda region, and the Australian region. Each OTU can be interpreted diferently depending on avail- able supporting information, either based on biological, ecological or geographical data. We found that SNP data pro- vided more robust results than mtDNA data in determining the boundary between population and cryptic species. Conclusion: To split a cryptic species complex and erect new species based purely on the results of genetic analyses is not recommended. The designation of new species needs supportive diagnostic morphological characters that allow for species recognition, as an inability to recognise individuals in the feld creates difculties for future research, management for conservation and fsheries purposes. Moreover, we recommend that future studies use a compre- hensive sampling regime that encompasses the full range of a species complex. This approach would increase the likelihood of identifcation of operational taxonomic units rather than resulting in an incorrect designation of new species. Keywords: Speciation, Species complex, Elasmobranch, Genetics Background Te development of genetic and genomic studies has substantially infuenced how species are defned taxo- nomically, with a shift from traditional taxonomy based *Correspondence: [email protected]; [email protected] on morphological and biological characters to one that 1 School of Biological Sciences, The University of Queensland, Brisbane, includes or entirely relies on DNA-evidence (e.g. [1]). QLD 4072, Australia Full list of author information is available at the end of the article While the necessity for phylogenetic support in defning © The Author(s) 2021. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Fahmi et al. BMC Ecol Evo (2021) 21:121 Page 2 of 16 a species is the subject of debate, many journals require visual discrimination are absent [12–14]. A lack of feld- phylogenetic analyses in the description of new taxa [2]. based identifcation may confound determination of a Advanced DNA sequencing has revealed species com- species’ conservation status, and management strategies plexes and cryptic species previously assumed to be that might be relevant for that species [6, 15, 16]. subspecies or populations of a single species through tra- Cryptic species are common in many groups of taxa ditional taxonomic analysis [3–5]. In evolutionary theory, and various habitats, including in marine environments species complexes are considered recently diverged from [4, 6, 17]. In elasmobranchs, the number of recognised evolving metapopulations [3, 6]. As an ongoing process cryptic species has increased substantially within the last of speciation, morphological diferentiation may develop decade, primarily due to a large, multi-taxa, phylogenetic later due to local adaptation to new environments [3, study of mitochondrial NADH2 sequences [18]. Several 4]. Cryptic species may be present within a complex putative cryptic species have been identifed with most when morphologically indistinguishable individuals are originating from areas of high geographic complexity, revealed to be genetically distinct [6–8]. While there are and in taxa with low dispersal ability [18, 19]. Te use of disparities in the defnition of cryptic species in terms of genome-wide approaches alongside mitochondrial mark- their biology, they provide challenges for taxonomic and ers has improved the ability to identify cryptic diversity evolutionary studies [9]. For instance, the discovery of of elasmobranchs (e.g. in mobulids [20]). cryptic species in what was previously considered a sin- In this study, we examined the brown-banded bam- gle wide-ranging species raises questions whether geo- booshark, Chiloscyllium punctatum, a species distrib- graphically-structured populations can be diferentiated uted in near-shore environments within the Indian and from diferent species within the same region, leading to the Western Pacifc Oceans [21–25] (Fig. 1), and the most taxonomic confusion [10, 11]. A reliance on genetic evi- commonly caught shark in coastal fsheries in Southeast dence alone to split a species complex into two or more Asia [26]. Previous genetic and morphological studies new species presents wildlife managers and ecologists have suggested that C. punctatum contains two cryptic with challenges as morphological features that facilitate species [18, 27]. However, the genetic study only included Fig. 1 Map showing the Chiloscyllium punctatum sample-collection locations. Abbreviations of location names refer to Table 2 Fahmi et al. BMC Ecol Evo (2021) 21:121 Page 3 of 16 (See fgure on next page.) Fig. 2 A Maximum likelihood (ML) tree based on the Tamura-Nei model analysis (TN93 G) of the NADH2 data with bootstrap support for + 1000 replicates. The outgroup is the congener species, Chiloscyllium plagiosum from West Kalimantan; B Median-joining haplotype network of Chiloscyllium punctatum from Indo Australian region. Circle diameter represents haplotype frequency, connecting lines represent single mutational steps, and hash marks represent the number of haplotypes a few sampling locations with uneven sample sizes and of haplotypes. Samples from the west coast of Suma- large geographic breaks, likely under-representing the spe- tra (WSA and WSS) formed a distinct haplotype, while cies’ genetic diversity within the region [17]. Here we use Papua New Guinea (PNG) and Australia (SEQ and genome-wide nuclear single nucleotide polymorphisms WAU) formed an Australian region cluster (Fig. 2B). (SNPs) along with mitochondrial DNA lineages to assess Te largest haplotype divergence (1.7–2.8%) occurred potential cryptic speciation within an extensive, previously between the Indo-Malay samples and those from the un-sampled area within the Indonesian archipelago, and to Australian region. Samples from the Indian Ocean evaluate the use of genetic and genomic data to delineate region (WSA, WSS, LMB and MUN) formed distinc- species. tive haplotypes separated from the Australian region by 0.5–1.4%. In contrast, samples from South Sulawesi Results (SUL) formed a diferent sub-cluster of the Indo-Malay Mitochondrial gene phylogeny haplotypes by 0.6–0.8%. In total, 34 individuals were sequenced for the mitochon- drial NADH2 marker across 12 locations. Two phyloge- netic analyses of the trimmed alignment sequence data SNP genotyping (1044 bp) (maximum likelihood phylogenetic tree and A total of 82,994 SNPs were detected from 148 indi- median-joining haplotype network) showed similar clus- viduals across 16 sampling locations. Filtering crite- terings of haplotypes (Fig. 2). Te phylogenetic tree indi- ria resulted in the subsequent reduction of SNP loci cated two major clades: (i) samples from Papua New to 6,099 SNP loci (see Additional fle 2) that was used Guinea (PNG), Australia (SEQ and WAU), Lombok (LMB), for the population structure and phylogenetic analyses. west coast of Sumatra (WSA and WSS), Muncar (MUN); All individuals clearly grouped into their geographical and (ii) samples from South East Asia including Tailand regions. A PCoA based on axis 1 (38.5% of the variation (PHU), Malaysia (PAH) and Indonesia (BIN, WKL, WJV, among individuals) and axis 2 (19.5%) showed three SUL). Within the frst clade, samples from Papua New main clusters for the C. punctatum-complex (Fig. 3A): Guinea and Australia formed a distinct cluster
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