Next Article in Journal
Fault-Tolerant Formation Control for Multiple Stochastic AUV System under Markovian Switching Topologies
Next Article in Special Issue
Impacts of the Establishment of Biofoulants on Greek Aquaculture: Farmers’ Expert Knowledge
Previous Article in Journal
The Construction and Application of Dual-Objective Optimal Speed Model of Liners in a Changing Climate: Taking Yang Ming Route as an Example
Previous Article in Special Issue
Value Chain for Non-Indigenous Bivalves in Greece: A Preliminary Survey for the Pearl Oyster Pinctada imbricata radiata
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
JMSE
Volume 11
Issue 1
10.3390/jmse11010158
jmse-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Phylogenetic Affinities of Acanthopleurinae Dall, 1889 Chitons (Mollusca: Polyplacophora: Chitonidae) from Jazan Coast in the Red Sea and Western Indo-Pacific

by
Hassien Alnashiri
1,
Liju Thomas
2,*,
Maqbool Thaikkottathil
1,
Siby Philip
3,
Ranjeet Kutty
4,
Sureshkumar Sivanpillai
2 and
Ali Mohammed Abo Rasain
1
1
Department of Biology, College of Science, Jazan University, Jazan 82817, Saudi Arabia
2
Faculty of Ocean Science and Technology, Kerala University of Fisheries and Ocean Studies, Kochi 682506, India
3
Department of Zoology, Nirmalagiri College, Kannur 670701, India
4
Department of Aquatic Environment Management, Kerala University of Fisheries and Ocean Studies, Kochi 682506, India
*
Author to whom correspondence should be addressed.
J. Mar. Sci. Eng. 2023, 11(1), 158; https://doi.org/10.3390/jmse11010158
Submission received: 31 October 2022 / Revised: 21 December 2022 / Accepted: 4 January 2023 / Published: 9 January 2023
(This article belongs to the Special Issue Marine Fish and Invertebrate Aquaculture)
Browse Figures
Versions Notes

Abstract

:
Chitons (Polyplacophora) are marine molluscs that mostly inhabit rocky intertidal shores. Their biological and phylogenetic studies are comparatively sparse in the western Indo-Pacific regions. In addition, chitons belonging to the subfamily Acanthopleurinae Dall, 1889, collected from the Andaman Sea of the northeastern Indian Ocean and the Jizan coast of Saudi Arabia were sequenced and analyzed to study the phylogenetic affinities. The analysis was carried out using a single locus dataset (cytochrome oxidase 1) generated during the present study and integrated with sequences retrieved from GenBank. Acanthopleura gemmata (Blainville, 1825) from India was linked to Acanthopleura vaillantii Rochebrune, 1882, from the Saudi Arabia coast. Squamopleura miles (Carpenter in Pilsbry, 1893) from the Indian coast forms a separate clade representing the genus. Furthermore, the results illustrate several significant instances of misplacement of several species under the wrong genus and the existence of cryptic species within the genera Acanthopleura and Squamopleura. An integrated approach is required to better understand these important intertidal groups’ taxonomy, systematics, and biogeography.

1. Introduction

The class Polyplacophora, with more than a thousand nominal species, is an ancient clade of extant molluscs, common in the intertidal and subtidal zones of tropical and temperate regions, with several representatives from the deep sea [1]. The chitons are considered taxonomically difficult [2] owing to their superficial resemblance in morphology within and between groups. In addition, using novel morphological and anatomical characters in conjunction with molecular phylogeny and population genetics data has revealed the cryptic diversity among chitons and led to the discovery of various new species [3,4,5]. In the past two decades, more than 200 species of chitons have been discovered and described globally. Monophyly of the two major lineages of Polyplacophora (Order Lepidopleurida and order Chitonida) has been resolved by morphological and molecular characteristics [2,6,7,8].
The subfamily Acanthopleurinae Dall, 1889 (family Chitonidae) is a group of medium- to large-sized chitons and is a common inhabitant along the rocky intertidal regions [9]. Acanthopleurinae are represented by 20 species (Table 1) grouped under four genera, viz. Acanthopleura Guilding, 1830, Enoplochiton Gray, 1847, Liolophura Pilsbry, 1893; and Squamopleura Nierstrasz, 1905 (MolluscaBase, 2022). The ecology, feeding behavior, reproduction, homing behavior, radular biomineralization, shell ocelli, and bioerosion [10,11,12,13,14,15,16,17] of several Acanthopleurinae species have already been characterized. However, the identification of species based on non-reliable morphological characters over detailed examination (characters on the tegmentum and perinotum), along with the lack of specimens from wide-ranging locations, add to the taxonomic complexity within several species groups of Acanthopleurinae [18,19,20].
A revision of the genus Acanthopleura by Ferreira (1986) identified Acanthopleura as the senior synonym of 13 genera [21]. Brooker studied the anatomy of Acanthopleura using a scanning electron microscope and included 16 species in the genus [22]. The revision resulted in 15 species, where he coalesced species from three other genera (Liolophura, Squamopleura, and Enoplochiton) into the genus Acanthopleura.
In the Western Indo-Pacific Polyplacophora has only four representatives: (Acanthopleura gemmata (Blainville, 1825), Acanthopleura brevispinosa (G. B. Sowerby II, 1840), Acanthopleura vaillantii (Rochebrune, 1882), and Squamopleura miles (Carpenter in Pilsbry, 1893)) [9]. A. gemmata has a wide distribution in the Indo-Pacific, from the Andaman Islands in the west to Tonga in the east, along the coasts of Australia and the northern Philippines [9], with records also from the East African coast [9]. A. brevispinosa is known to be distributed along the east African coast from Somalia to Mozambique and along the coasts of the Seychelles, Comoro Islands, Madagascar, Reunion, and Mauritius [9]. A. vaillantii shows distribution along the shores of the Red Sea, Yemen, and Socotra Island to the opening of the Arabian Gulf, and the distributional records of S. miles in the western Indo-Pacific are from Sri Lanka in the west to New Guinea in the east and from Taiwan in the north to Australia in the south [9].
The studies on chitons from the western Indo-Pacific are limited compared to other regions. Several researchers have recently studied chitons from the region, primarily focusing on the taxonomy, diversity, and distribution [23,24,25,26,27,28,29,30,31,32,33,34,35,36,37]. However, no works on taxonomy and systematics based on molecular techniques are available.
In this study, a molecular taxonomic study is undertaken to elucidate the phylogenetic affinities of Acanthopleurinae chitons from the Western Indo-Pacific using the universal barcoding locus and the partial mitochondrial cytochrome oxidase 1 (COI) gene sequence data.

2. Materials and Methods

2.1. Sampling

The specimens were collected from the intertidal zone along the coast of the Andaman and Nicobar Islands, India (A. gemmata and S. miles), and Saudi Arabia’s coast of the Red Sea (A. vaillantii) during 2020–2021 (Table 2). The specimens were collected by hand from crevices in the exposed rocks during low tide.

2.2. DNA Extraction, PCR Amplification, and Sequencing

The genomic DNA was extracted from ethanol-preserved specimens using the DNeasy Blood and Tissue Kit (Qiagen, Hilden, Germany) using the Qiagen QIAcube HT DNA extraction automation system, following the manufacturer’s instructions. The partial sequence of the mitochondrial cytochrome oxidase 1 (COI) marker was amplified using the LCO1490 and HCO2198 primers [38]. The PCR amplification was carried out in a 25 µL master mix consisting of 15.4 µL dd H2O, 5 µL 10× buffer (Invitrogen, Waltham, MA, USA), 0.35 µL MgCl2 (Applied Biosystems, Waltham, MA, USA), 0.5 µL of 10 mM dNTPs (Promega, Madison, WI, USA), 1.25 µL of 0.1 µM of each primer, 0.25 µL of 5 U/µL Taq Polymerase (Invitrogen, Waltham, MA, USA) and 1 µL of DNA template. The thermal cycler was programmed for 35 cycles of 94 °C for 60 s, 49 °C for 90 s and 72 °C for 90 s, after an initial denaturation of 95 °C for 5 min. The reaction mixture was subjected to a final elongation of 72 °C for 6 min and held at 4 °C until further steps were taken. The amplified PCR products are purified using Wizard® SV Gel and PCR Clean-Up System (Promega), following the manufacturer’s protocol, and outsourced for deep sequencing.

2.3. Sequence Selection and Analysis

In this study, 67 sequences of chitons belonging to the subfamily Acanthopleurinae were assembled. A total of eight sequences were generated for three species from the western Indo-Pacific. The rest of the sequences were retrieved from the GenBank and BOLD databases (Table 3). The sequences generated from the present study were also submitted to GenBank (OM758201-OM758209). In addition, the sequences were aligned using MUSCLE [39] as implemented in SeaView v5.0.5 [40]. The data were partitioned to three codon positions of the COI gene to create a full partition, and a partition analysis [41] and ModelFinder [42] were used to find the right partitioning scheme and the best-fit substitution model. The maximum likelihood (ML) analysis was performed using IQ-TREE [43] with the best partition scheme and ultrafast bootstrap support for 1000 iterations [44]. The phylogenetic tree was edited and visualized in FigTree v1.4.4 [45].

3. Results

The present study incorporates 14 of the 20 valid species belonging to four genera under the subfamily Acanthopleurinae. The partition analysis suggested separate nucleotide substitution models for three codon positions of the COI gene, with TIM3 + F + I + G4 for the first codon position (BIC = 2105.7466, lnL = −1028.4610), F81 + F + I (BIC = 761.5852, lnL = −367.2302) for the second codon position, and HKY + F + G4 for the third codon position (BIC = 8249.4081, lnL = −4108.4292).
A total of four distinct clades (‘Enoplochiton’, ‘Acanthopleura’, ‘Squamopleura’, and ‘Liolophura’) representing four genera under the subfamily Acanthopleurinae were resolved in ML analysis (Figure 1). Several species presently included in Acanthopleura and Liolophura were found to be placed across different genera. Based on the analysis, our study demonstrates the occurrence of cryptic species within the genera Acanthopleura and Squamopleura, respectively (see Figure 1).
The results of the present analysis also provide insights into the biogeography of Acanthopleurinae chitons. The majority of species in our study are from the Indo-Pacific region. All the species in the clade ‘Acanthopleura’ are recorded from the Indo-Pacific except Acanthopleura granulata (Gmelin, 1791), which is recorded from the Caribbean. The clades ‘Liolophura’ and ‘Squamopleura’ include species from the Indo-Pacific, while the species of the clade ‘Enoplochiton’ are restricted along the west coast of South America (Figure 2).

4. Discussion

The phylogenetic affinities of Acanthopleurinae chitons from the western Indo-Pacific were addressed in the present study. The study focused on the phylogenetic relationships of Acanthopleurinae chitons from the western Indo-Pacific. Based on the phylogenetic analysis and morphological characters, the three species collected in the present study belonged to the subfamily Acanthopleurinae. A. gemmata from the Andaman coast and A. vaillantii from the Red Sea were related and thus belonged to the genus Acanthopleura, while S. miles from the Andaman coast was grouped under the genus Squamopleura. The results also illustrate the ambiguity in the misplacement of several species under the wrong genus and the existence of cryptic species within the genera Acanthopleura and Squamopleura. The incorrect placement of species could be due to wrong identification prior to sequencing and deposition of the sequences in the GenBank (HM180654, MH587607), and those within the subfamily could be due to a lack of detailed analysis using more advanced taxonomic tools [5].

4.1. Phylogenetic Affinities of Acanthopleurinae

As per the current understanding, the subfamily Acanthopleurinae accommodates 20 validated species belonging to four genera. The present analysis resolves the species of Acanthopleurinae across four clades representing the four genera (Figure 1).

4.1.1. Acanthopleura Guilding, 1830

According to our present knowledge, Acanthopleura is globally represented by eight species, with distributional records from the western part of the Indian Ocean to the central part of the Pacific and the western coast of South America and the Caribbean Sea [9]. Based on our analysis, species currently validated under the genus Acanthopleura are resolved across three clades. The majority of the species currently validated under the nominal genus Acanthopleura are included in the clade ‘Acanthopleura’. The placement of the type species Acanthopleura spinosa (Bruguière, 1792) separately from the rest of the species in the sequence is controversial and requires verification using more data. Acanthopleura loochooana (Broderip & G. B. Sowerby I, 1829) was conventionally placed under the genus Acanthopleura. The three sequences from the database (AB066223, MT585716, and MT585719) are included in the clade ‘Squamopleura’ in the present study (Figure 1). Another sequence (MH587607) recorded as A. loochooana is a misidentification and falls outside the subfamily Acanthopleurinae. More data is therefore required to ascertain the right placement of this species. The sequences of Acanthopleura echinata (Barnes, 1824) from the western coast of South America have shown affinity for the clade ‘Enoplochiton’ rather than ‘Acanthopleura’ (Figure 1). Brooker [22], who suggested the placement of A. echinata under the genus Enoplochiton, supports the results of the present study. Likewise, two sequences (AB065288 and AB066223) that have been reported as A. tenuispinosa and A. miles, are misidentified specimens, under the genus Acanthopleura. However, in our study, we found their affinity towards the genera Liolophura and Squamopleura, respectively. The results also demonstrate the probable occurrence of cryptic species within the species currently identified as A. gemmata from the coasts of India (Andaman Islands), Malaysia (Penang), and Japan. The specimen of A. gemmata collected from the Indian coast has a genetic distance of 10.6% and 3.0% with specimens recorded from Japan and Malaysia, respectively. The type locality of A. gemmata is Australia (New Holland), and the unavailability of molecular data from the type locality prevents us from identifying the nominal species from the Andaman Islands. A recent study on Acanthopleurinae chitons from Indonesia [19] also highlighted the probably hidden diversity of Acanthopleura. The phylogeny of the rest of the Acanthopleura species is resolved within the clade.

4.1.2. Liolophura Pilsbry, 1893

Recent studies on genetic polymorphisms [4] and species discrimination with geographical distribution patterns and divergence [5] of Liolophura japonica (Lischke, 1873) from the northwestern Pacific revealed the existence of cryptic species and resulted in the description of two new species (Liolophura koreana Yeo & U. W. Hwang, 2021, and Liolophura sinensis Choi, B. Park & U. W. Hwang, 2021) [5]. Five species of Liolophura were not represented in our analysis due to the unavailability of data: Liolophura arenosa (Ferreira, 1986), Liolophura hirtosa (Péron MS, Blainville, 1825), Liolophura rehderi (Ferreira, 1986), Liolophura gaimardi (Blainville, 1825), and Liolophura tenuispinosa (Leloup, 1939) [20]. However, sequences of Acanthopleura gaimardi (AB066221, LIMX064, LIMX065, and LIMX097) in our study fall in the clade ‘Acanthopleura’ indicating that the taxonomically accepted L. gaimardi could be a species of the genus Acanthopleura. More specimens of the species need to be verified with morphological and molecular tools before placing them in the clade ‘Acanthopleura’. The sequence (HM180654) seems misidentified as it falls out of the subfamily Acanthopleurinae.

4.1.3. Squamopleura Nierstrasz, 1905

Globally, the genus Squamopleura is represented by three valid species (see Table 1). The type species, Squamopleura miles (Carpenter in Pilsbry, 1893) is known to have a wide distribution from Sri Lanka in the west to New Guinea in the east, and from Taiwan in the north to north-western Australia in the south [9]. The species recorded as S. miles from the Andaman Islands in the present study, however, aligned with A. miles from Japan (AB064988), indicating that the latter could be a misidentification as they fall entirely outside of the clade ‘Acanthopleura’. This indicates that there could be an occurrence of a species complex for S. miles since the sequence from the Indian coast has a genetic distance of above 9% from those recorded from Japanese waters. Starger [19] identified the existence of cryptic species of Squamopleura in Indonesian waters. The two species of the genus that are not represented in our analysis are Squamopleura araucariana (Hedley, 1898) and Squamopleura curtisiana (E. A. Smith, 1884). Another noteworthy observation relates to the placement of Acanthopleura loochooana under the clade ‘Squamopleura.’ This needs further study to ascertain the systematics of this species.

4.1.4. Enoplochiton Gray, 1847

The genus Enoplochiton, restricted to the central part of the western coast of South America, is presently represented by a single species, Enoplochiton niger (Barnes, 1824). The present analysis suggests the placement of A. echinata and E. niger in the clade ‘Enoplochiton’. Both E. niger and A. echinata belong to the same geographical region, along the west coast of South America, suggesting that this phylogenetic replacement is reasonable. A detailed examination of morphological characters is required to justify the placement of A. echinata under the genus Enoplochiton.

4.2. Acanthopleurinae in the Western Indo-Pacific

Research suggests that three species of Acanthopleura (A. brevispinosa, A. gemmata, and A. vaillantii) and a single species of Squamopleura (S. miles) represent the diversity of Acanthopleurinae from the Western Indo-Pacific. Our analysis suggests the probability of having more species of Acanthopleura and Squamopleura from the western Indo-Pacific, reflecting the geographical distribution patterns as inferred by previous studies [5,18]. Population genetic analysis using COI and 16S genes on the genus Liolophura from the northwestern Pacific coast revealed the occurrence of three species lineages [5]. Along with genetic studies, morphological analysis using field emission scanning electron microscopy (FE-SEM) identified differences in the black spots on the tegmentum and spicules on the perinotum, resulting in the discovery of two new species (L. koreana and L. sinensis), along with the previously known L. japonica [5]. An integrated approach using morphological characters and molecular data from different locations along the Western Indo-Pacific could provide interesting insights into the cryptic diversity of Acanthopleurinae.

5. Conclusions

The rich diversity of chitons also poses a significant challenge for the taxonomists to classify them accordingly. As discussed above, there is a need for an integrated taxonomic approach for identifying many species that show morphological similarities. In our present study, we have made an attempt to understand the complexity of the taxonomic status of species in the subfamily Acanthopleurinae based on molecular analysis using a single locus dataset. Though we understand this is not a comprehensive approach, based on the available data, we have made an attempt to shed light on certain uncertainties in the taxonomy and systematics of certain species from the Western Indo-Pacific region. The analysis also confirms the existence of cryptic diversity within the genus Acanthopleura. As a result of their preference for intertidal habitats, chitons form an interesting model for understanding the fluxes in the intertidal zone caused by destructive environmental and climatic events. An integrated approach using morphological and molecular tools with improved sampling and data generation will provide a better understanding of these important intertidal groups’ taxonomy, systematics, and biogeography.

Author Contributions

M.T. and L.T. set up and performed the lab experiments, interpreted the data results, and wrote the manuscript. S.P. and R.K. contributed to and supported the lab’s experiments. S.S., A.M.A.R. and H.A. contributed to analyzing and inspecting the data and editing the manuscript. H.A., L.T. and M.T. gave the idea for a research project and planned the experiments; they also analyzed and inspected the data and edited the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

Deputyship for Research & Innovation, Ministry of Education in Saudi Arabia, Project Number No. 11613.

Institutional Review Board Statement

The animal study protocol was approved by the Ethics Committee of Department of Biology, College of Science, Jazan University.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data is contained within the article.

Acknowledgments

The authors extend their appreciation to the Deputyship for Research & Innovation, Ministry of Education in Saudi Arabia, for funding this research work through project number (No. 11613) under the Research Groups program of Jazan University for the Ministry of Education’s Institutional Support Program ISP20-22. Our appreciation also goes to the Deanship of Scientific Research at Jazan University for their efforts in organizing and supporting this project. Liju Thomas is funded by the Council for Scientific and Industrial Research (CSIR), Senior Research Fellowship (SRF direct). We acknowledge Ramvilas Ghosh (Kerala University of Fisheries and Ocean Studies) for the assistance in sampling from the Indian coast and Shalu Kannan (Kerala University of Fisheries and Ocean Studies) for preparing the study area map.

Conflicts of Interest

The authors declare that there is no conflict of interest regarding the publication of this article.

References

  1. MolluscaBase Editors. MolluscaBase. Available online: https://www.molluscabase.org/ (accessed on 12 July 2022).
  2. Sigwart, J.D.; Stoeger, I.; Knebelsberger, T.; Schwabe, E. Chiton phylogeny (Mollusca: Polyplacophora) and the placement of the enigmatic species Choriplax grayi (H. Adams & Angas). Invertebr. Syst. 2013, 27, 603. [Google Scholar] [CrossRef]
  3. Sigwart, J.D.; Chen, C. Life history, patchy distribution, and patchy taxonomy in a shallow-water invertebrate (Mollusca: Polyplacophora: Lepidopleurida). Mar. Biodivers. 2018, 48, 1867–1877. [Google Scholar] [CrossRef] [Green Version]
  4. Xu, H.; Chu, Z.; Zhang, J.; Jing, M.; Huang, L. Genetic Diversity and Population Structure of Acanthochiton rubrolineatus (Polyplacophora) Based on Mitochondrial and Nuclear Gene Markers. Diversity 2020, 12, 159. [Google Scholar] [CrossRef] [Green Version]
  5. Choi, E.H.; Yeo, M.Y.; Kim, G.; Park, B.; Shin, C.R.; Baek, S.Y.; Hwang, U.W. Liolophura Species Discrimination with Geographical Distribution Patterns and Their Divergence and Expansion History on the Northwestern Pacific Coast. Sci Rep 2021, 11, 17602. [Google Scholar] [CrossRef] [PubMed]
  6. Sirenko, B.I. Revision of the system of the order Chitonida (MoBusca: Polyplacophora) on the basis of correlation between the type of gills arrangement and the shape of the chorion processes. Ruthenica. 1993, 3, 93–119. [Google Scholar]
  7. Okusu, A.; Schwabe, E.; Eernisse, D.J.; Giribet, G. Towards a phylogeny of chitons (Mollusca, Polyplacophora) based on combined analysis of five molecular loci. Org. Divers. Evol. 2003, 3, 281–302. [Google Scholar] [CrossRef] [Green Version]
  8. Sirenko, B. New Outlook on the System of Chitons (Mollusca: Polyplacophora). Venus 2006, 65, 27–49. [Google Scholar] [CrossRef]
  9. Kaas, P.; Van Belle, R.A.; Strack, H.L. Monograph of Living Chitons (Mollusca: Polyplacophora); Brill: Leiden, The Netherlands, 2006; Volume 6, pp. 1–464. ISBN 9789004115781. [Google Scholar]
  10. Thorne, M. Studies on Homing in the Chiton Acanthozostera gemmata. Mar. Freshw. Res. 1968, 19, 151–160. [Google Scholar] [CrossRef]
  11. Chelazzi, G.; Focardi, S.; Deneubourg, J.L. A Comparative Study on the Movement Patterns of Two Sympatric Tropical Chitons (Mollusca: Polyplacophora). Mar. Biol. 1983, 74, 115–125. [Google Scholar] [CrossRef]
  12. Chelazzi, G.; Focardi, S.; Louis Deneubourg, J.; Innocenti, R. Competition for the home and aggressive behavior in the chiton Acanthopleura gemmata (Blainville) (Mollusca: Polyplacophora). Behav. Ecol. Sociobiol. 1983, 14, 15–20. [Google Scholar] [CrossRef]
  13. Kim, K.-S.; Macey, D.J.; Webb, J.; Mann, S. Iron mineralization in the radula teeth of the chiton Acanthopleura hirtosa. Proc. R. Soc. Lond. Ser. B Boil. Sci. 1989, 237, 335–346. [Google Scholar] [CrossRef]
  14. Barbosa, S.S.; Byrne, M.; Kelaher, B.P. Bioerosion Caused by Foraging of the Tropical Chiton Acanthopleura gemmata at One Tree Reef, Southern Great Barrier Reef. Coral Reefs 2008, 27, 635–639. [Google Scholar] [CrossRef]
  15. Brooker, L.R.; Shaw, J.A. The Chiton Radula: A Unique Model for Biomineralization Studies. Advanced Topics in Biomineralization; IntechOpen: London, UK, 2012; pp. 65–84. ISBN 9789535100454. [Google Scholar]
  16. Saunders, M.; Kong, C.; Shaw, J.A.; Macey, D.J.; Clode, P.L. Characterization of Biominerals in the Radula Teeth of the Chiton, Acanthopleura hirtosa. J. Struct. Biol. 2009, 167, 55–61. [Google Scholar] [CrossRef] [Green Version]
  17. Varney, R.M.; Speiser, D.I.; McDougall, C.; Degnan, B.M.; Kocot, K.M. The Iron-Responsive Genome of the Chiton Acanthopleura granulata. Genome Biol. Evol. 2021, 13, evaa263. [Google Scholar] [CrossRef]
  18. Okoshi, K.; Hamaguchi, M. Two Morphological and Genetic Forms of the Japanese Chiton Acanthopleura Japonica. Venus 2006, 65, 113–122. [Google Scholar] [CrossRef]
  19. Starger, C.; Eernisse, D.J.; Brooker, L.R.; Yusmalinda, A.; Arlyza, I.; Mahardika, G.N.; Toha, A.H.; Ambariyanto; Barber, P. DNA barcoding Indonesian Acanthopleurinae (Polyplacophora). In Proceedings of the 17th World Congress of Malacology, Phuket, Thailand, 18–24 July 2010. [Google Scholar]
  20. Jardim, J.; Almeida, S.; Simone, L. Towards Understanding a Confusing and Widespread Species: An Anatomical Study of Acanthopleura gemmata (Polyplacophora, Chitonidae) from Thailand. Strombus 2020, 26, 1–14. [Google Scholar]
  21. Ferreira, A.J. A Revision of the Genus Acanthopleura Guilding, 1829 (Mollusca: Polyplacophora). Veliger 1986, 28, 221–279. [Google Scholar]
  22. Brooker, L.R. Revision of Acanthopleura Guilding, 1829 (Mollusca: Polyplacophora) Based on Light and Electron Microscopy. Ph.D. Thesis, Murdoch University, Perth, Australia, 2003. [Google Scholar]
  23. Dell’Angelo, B.; Bonfitto, A.; Taviani, M.; Sabelli, B. Chitons (Mollusca, Polyplacophora) from Bioclastic Sands of the Ifaty-Tuléar Back Reefs (Madagascar, Western Indian Ocean). Boll. Malacol. 2004, 5, 45–62. [Google Scholar]
  24. Dell’Angelo, B.; Sabelli, B.; Taviani, M.; Bonfitto, A. New Data on the Polyplacophora of Madagascar (Western Indian Ocean). Arch. Für Molluskenkd. Int. J. Malacol. 2010, 139, 35–43. [Google Scholar] [CrossRef]
  25. Dell’angelo, B.; Gori, S.; Baschieri, L.; Bonfitto, A. Chitons (Mollusca, Polyplacophora) from the Maldive Islands. Zootaxa 2010, 2673, 1–38. [Google Scholar] [CrossRef]
  26. Dell’Angelo, B.; Prelle, G.; Sosso, M.; Bonfitto, A. Intertidal Chitons (Mollusca: Polyplacophora) from Southern Madagascar. Afr. Invertebr. 2011, 52, 21–37. [Google Scholar] [CrossRef]
  27. Dell’Angelo, B.; Prelle, G.; Sosso, M.; Bonfitto, A. A New Species of Callochiton (Mollusca: Polyplacophora) from Southern Madagascar. Molluscan Res. 2012, 32, 154–158. [Google Scholar]
  28. Dell’Angelo, B.; Sirenko, B.; Prelle, G. A New Species of Stenoplax (Mollusca: Polyplacophora: Ischnochitonidae) from Southern Madagascar. Boll. Malacol. 2015, 51, 91–96. [Google Scholar]
  29. Dell’Angelo, B.; Landau, B.M.; Sosso, M.; Taviani, M. Late Pleistocene Red Sea Mollusca: 1. Polyplacophora. Zootaxa 2020, 4772, 401–449. [Google Scholar] [CrossRef] [PubMed]
  30. Anseeuw, B.; Terryn, Y. Intertidal Chitons (Mollusca: Polyplacophora) from the Coast of Jordan, Red Sea, with the Description of a New Species of Parachiton Thiele, 1909. Boll. Malacol. 2004, 5, 1–24. [Google Scholar]
  31. Schwabe, E. The Polyplacophora (Mollusca) Collected during the First International Marine Biodiversity Workshop for Rodrigues (Western Indian Ocean), with the Description of a New Species. J. Nat. Hist. 2004, 38, 3143–3173. [Google Scholar] [CrossRef]
  32. Schwabe, E. Chitons (Mollusca, Polyplacophora) Collected during the Thai-Danish Bioshelf Surveys (1996–2000) in the Andaman Sea, Indian Ocean. J. Zool. Soc. Wallacea 2006, 2, 19–28. [Google Scholar]
  33. Schwabe, E. Taxonomic Notes on Chitons. 5*. On Some Problematica and a New Record of Polyplacophora from Indonesia. (Mollusca). Spixiana 2007, 30, 145–158. [Google Scholar]
  34. Schwabe, E.; Els, R. The Genus Craspedochiton (Mollusca: Polyplacophora: Acanthochitonidae) in South African Waters: What Do We Really Know about It? Arch. Für Molluskenkd. 2019, 148, 73–92. [Google Scholar] [CrossRef]
  35. Dinapoli, A.; Janssen, R. Polyplacophora (Mollusca) of the Socotra Archipelago—Systematics and Biogeography. Fauna Arab. 2009, 24, 1–46. [Google Scholar]
  36. Sirenko, B.I.; Schwabe, E. Description of a Minute New Chiton (Mollusca, Polyplacophora) from Sri Lanka. Ruthenica 2011, 21, 113–121. [Google Scholar]
  37. Sirenko, B.I. Two New Leptochitons (Mollusca, Polyplacophora, Leptochitonidae) from Madagascar and Mozambique. Zool. Zhurnal 2019, 98, 845–853. [Google Scholar] [CrossRef]
  38. Folmer, R.H.A.; Nilges, M.; Folkers, P.J.M.; Konings, R.N.H.; Hilbers, C.W. A Model of the Complex between Single-Stranded DNA and the Single-Stranded DNA Binding Protein Encoded by Gene V of Filamentous Bacteriophage M13. J. Mol. Biol. 1994, 240, 341–357. [Google Scholar] [CrossRef]
  39. Edgar, R.C. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004, 32, 1792–1797. [Google Scholar] [CrossRef] [Green Version]
  40. Gouy, M.; Guindon, S.; Gascuel, O. SeaView Version 4: A Multiplatform Graphical User Interface for Sequence Alignment and Phylogenetic Tree Building. Mol. Biol. Evol. 2010, 27, 221–224. [Google Scholar] [CrossRef] [Green Version]
  41. Chernomor, O.; von Haeseler, A.; Minh, B.Q. Terrace Aware Data Structure for Phylogenomic Inference from Supermatrices. Syst. Biol. 2016, 65, 997–1008. [Google Scholar] [CrossRef] [Green Version]
  42. Kalyaanamoorthy, S.; Minh, B.Q.; Wong, T.K.F.; von Haeseler, A.; Jermiin, L.S. ModelFinder: Fast Model Selection for Accurate Phylogenetic Estimates. Nat. Methods 2017, 14, 587–589. [Google Scholar] [CrossRef] [Green Version]
  43. Nguyen, L.-T.; Schmidt, H.A.; von Haeseler, A.; Minh, B.Q. IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies. Mol. Biol. Evol. 2015, 32, 268–274. [Google Scholar] [CrossRef]
  44. Hoang, D.T.; Chernomor, O.; von Haeseler, A.; Minh, B.Q.; Vinh, L.S. UFBoot2: Improving the Ultrafast Bootstrap Approximation. Mol. Biol. Evol. 2018, 35, 518–522. [Google Scholar] [CrossRef]
  45. Rambaut, A. FigTree. Version 1.4.3. Available online: http://tree.bio.ed.ac.uk/software/ (accessed on 29 October 2022).
  46. Jaksch, K.; Eschner, A.; Rintelen, T.V.; Haring, E. DNA analysis of molluscs from a museum wet collection: A comparison of different extraction methods. BMC Res. Notes 2016, 9, 1–12. [Google Scholar] [CrossRef] [Green Version]
  47. Ibáñez, C.M.; Pardo-Gandarillas, M.C.; Méndez, M.A.; Sellanes, J.; Sigwart, J.D.; Sirenko, B. Phylogenetic position and morphological descriptions of Chiton species from the south-eastern Pacific. Zool. J. Linn. Soc. 2021, 191, 695–719. [Google Scholar] [CrossRef]
  48. Kim, D.W.; Yoo, W.G.; Park, H.C.; Yoo, H.S.; Kang, D.W.; Jin, S.D.; Lim, J. DNA barcoding of fish, insects, and shellfish in Korea. Genomics Inform. 2012, 10, 206–211. [Google Scholar] [CrossRef] [PubMed]
  49. Wu, X.; Zhang, H.; Yu, H.; Peng, X.; Zhang, Y. Genetic polymorphisms of Liolophura japonica among the southern of Zhejiang Province based on DNA barcoding. Mar. Fish 2018, 40, 265–278. [Google Scholar]
Jmse 11 00158 g001 550
Figure 1. Phylogenetic tree of Acanthopleurinae chitons constructed using cytochrome oxidase c subunit I.
Figure 1. Phylogenetic tree of Acanthopleurinae chitons constructed using cytochrome oxidase c subunit I.
Jmse 11 00158 g001
Jmse 11 00158 g002 550
Figure 2. Map showing the sampling locations and the geographical distribution of species from four genera used in the present analysis.
Figure 2. Map showing the sampling locations and the geographical distribution of species from four genera used in the present analysis.
Jmse 11 00158 g002
Table
Table 1. Species belonging to the subfamily Acanthopleurinae have been identified in different studies.
Table 1. Species belonging to the subfamily Acanthopleurinae have been identified in different studies.
Accepted Name (MolluscaBase)Ferreira, 1986Brooker, 2003Kaas et al. 2006
Acanthopleura brevispinosa (G. B. Sowerby II, 1840)Acanthopleura brevispinosaAcanthopleura brevispinosaAcanthopleura brevispinosa
Acanthopleura echinata (Barnes, 1824)Acanthopleura echinataEnoplochiton echinatusAcanthopleura echinata
Acanthopleura gemmata (Blainville, 1825)Acanthopleura gemmataAcanthopleura (Gemmata) gemmataAcanthopleura gemmata
Acanthopleura granulata (Gmelin, 1791)Acanthopleura granulataAcanthopleura (Gemmata) granulataAcanthopleura granulata
Acanthopleura loochooana (Broderip & G. B. Sowerby I, 1829)Acanthopleura loochooanaAcanthopleura (Squamopleura) loochooanaAcanthopleura loochooana
Acanthopleura planispina Bergenhayn, 1933Acanthopleura gemmata
Acanthopleura spinosa (Bruguière, 1792)Acanthopleura spinosaAcanthopleura spinosaAcanthopleura spinosa
Acanthopleura vaillantii Rochebrune, 1882Acanthopleura gemmataAcanthopleura vaillantiiAcanthopleura vaillantii
Enoplochiton niger (Barnes, 1824)Acanthopleura nigraEnoplochiton nigerEnoplochiton niger
Liolophura arenosa (Ferreira, 1986)Acanthopleura arenosaAcanthopleura arenosaLiolophura (Liolophura) arenosa
Liolophura gaimardi (Blainville, 1825)Acanthopleura gaimardiAcanthopleura (Liolophura) gaimardiLiolophura (Liolophura) gaimardi
Liolophura hirtosa (Péron MS, Blainville, 1825)Acanthopleura hirtosaAcanthopleura (Squamopleura) hirtosaLiolophura (Clavarizona) hirtosa
Liolophura japonica (Lischke, 1873)Acanthopleura japonicaAcanthopleura (Liolophura) japonicaLiolophura (Liolophura) japonica
Liolophura koreana Yeo & U. W. Hwang, 2021
Liolophura rehderi (Ferreira, 1986)Acanthopleura rehderiOnithochiton rehderiLiolophura (Liolophura) rehderi
Liolophura sinensis Choi, B. Park & U. W. Hwang, 2021
Liolophura tenuispinosa Leloup, 1939Liolophura tenuispinosaAcanthopleura (Liolophura) tenuispinosa
Squamopleura araucariana (Hedley, 1898)Acanthopleura araucarianaAcanthopleura (Squamopleura) araucarianaSquamopleura araucariana
Squamopleura curtisiana (E. A. Smith, 1884)Acanthopleura curtisianaAcanthopleura (Squamopleura) curtisianaSquamopleura curtisiana
Squamopleura miles (Carpenter in Pilsbry, 1893)Acanthopleura milesAcanthopleura (Squamopleura) milesSquamopleura miles
Acanthopleura (Gemmata) sp nov
Table
Table 2. Details of sampling locations.
Table 2. Details of sampling locations.
SpeciesLocalityLatitude, LongitudeNo. of Samples
Acanthopleura gemmataAndaman Islands, India11°34′44.8″ N 92°44′30.0″ E3
Acanthopleura vaillantiiJazan, Saudi Arabia16°56′39.3″ N 42°32′33.0″ E2
Squamopleura milesAndaman, Islands, India11°34′44.8″ N 92°44′30.0″ E2
Table
Table 3. Accession numbers and sources of sequences of COI used in the present study were retrieved from NCBI GenBank. Sequences retrieved from the BOLD database are mentioned as (BIN).
Table 3. Accession numbers and sources of sequences of COI used in the present study were retrieved from NCBI GenBank. Sequences retrieved from the BOLD database are mentioned as (BIN).
SpeciesLocationAccession NumberSource
Acanthochitona mahensis Winckworth, 1927Mahe, IndiaOM758209Present study
Acanthopleura brevispinosa (G. B. Sowerby II, 1840)Suez, EgyptKX537628[46]
Acanthopleura echinata (Barnes, 1824)Quintero, ChileMN864062[47]
Acanthopleura echinata (Barnes, 1824)Paracas, PeruMK016459[47]
Acanthopleura echinata (Barnes, 1824)Paracas, PeruMK016460[47]
Acanthopleura echinata (Barnes, 1824)Paracas, PeruMK016461[47]
Acanthopleura gaimardi (Blainville, 1825)Queensland, AustraliaAB066221Unpublished
Acanthopleura gaimardi (Blainville, 1825)UnknownLIMX064 (BIN)Unpublished
Acanthopleura gaimardi (Blainville, 1825)UnknownLIMX065 (BIN)Unpublished
Acanthopleura gaimardi (Blainville, 1825)UnknownLIMX097 (BIN)Unpublished
Acanthopleura gemmata (Blainville, 1825)Okinawa, JapanAB066222Unpublished
Acanthopleura gemmata (Blainville, 1825)Penang, MalaysiaMK016466[47]
Acanthopleura gemmata (Blainville, 1825)Penang, MalaysiaMK016467[47]
Acanthopleura gemmata (Blainville, 1825)Penang, MalaysiaMK016468[47]
Acanthopleura gemmata (Blainville, 1825)South Andaman, IndiaOM758201Present study
Acanthopleura gemmata (Blainville, 1825)South Andaman, IndiaOM758202Present study
Acanthopleura gemmata (Blainville, 1825)South Andaman, IndiaOM758203Present study
Acanthopleura granulata (Gmelin, 1791)UnknownAY377719[7]
Acanthopleura granulata (Gmelin, 1791)UnknownMZ467321Unpublished
Acanthopleura loochooana (Broderip & G. B. Sowerby I, 1829)UnknownMT585716Unpublished
Acanthopleura loochooana (Broderip & G. B. Sowerby I, 1829)UnknownMT585719Unpublished
Acanthopleura loochooana (Broderip & G. B. Sowerby I, 1829)Okinawa, JapanAB066223Unpublished
Acanthopleura loochooana (Broderip & G. B. Sowerby I, 1829)UnknownMH587607Unpublished
Acanthopleura miles (Carpenter in Pilsbry, 1893)Okinawa, JapanAB064988Unpublished
Acanthopleura planispina Bergenhayn, 1933Chichijima Island, JapanAB706351Unpublished
Acanthopleura spinosa (Bruguière, 1792)Miyako Island, JapanAB099505Unpublished
Acanthopleura tenuispinosa Leloup, 1939Okinawa, JapanAB065288Unpublished
Acanthopleura vaillantii Rochebrune, 1882Jazan, Saudi ArabiaOM758207Present study
Acanthopleura vaillantii Rochebrune, 1882Jazan, Saudi ArabiaOM758208Present study
Americoliva sayana (Ravenel, 1834)UnknownMZ091415Unpublished
Enoplochiton niger (Barnes, 1824)Iquique, ChileMK016414[47]
Enoplochiton niger (Barnes, 1824)Iquique, ChileMK016415[47]
Enoplochiton niger (Barnes, 1824)Iquique, ChileMK016419[47]
Lepidozona coreanica (Reeve, 1847)UnknownMT070411Unpublished
Ischnochiton hakodadensis P. P. Carpenter, 1893Hakkaido, JapanLC214409Owada, 2018
Liolophura japonica (Lischke, 1873)UnknownMT585720Unpublished
Liolophura japonica (Lischke, 1873)UnknownMT585718Unpublished
Liolophura japonica (Lischke, 1873)Ehime, JapanAB064986Unpublished
Liolophura japonica (Lischke, 1873)Tsushima, JapanKT932897[5]
Liolophura japonica (Lischke, 1873)Tsushima, JapanKT932890[5]
Liolophura japonica (Lischke, 1873)South KoreaJX503058Unpublished
Liolophura japonica (Lischke, 1873)UnknownAY377717[7]
Liolophura japonica (Lischke, 1873)UnknownHM180654[48]
Liolophura japonica (Lischke, 1873)Wakayama, JapanAB066269Unpublished
Liolophura japonica (Lischke, 1873)Zhejiang, ChinaMF774404[49]
Liolophura japonica (Lischke, 1873)Zhejiang, ChinaMG203946[49]
Liolophura japonica (Lischke, 1873)Zhejiang, ChinaMF774400[49]
Liolophura japonica (Lischke, 1873)Geojedo, South KoreaKT932872[5]
Liolophura japonica (Lischke, 1873)Tongyeong, South KoreaKT932867[5]
Liolophura japonica (Lischke, 1873)Tongyeong, South KoreaKT932866[5]
Liolophura japonica (Lischke, 1873)Geojedo, South KoreaKT932875[5]
Squamopleura miles (Carpenter in Pilsbry, 1893)South Andaman, IndiaOM758204Present study
Squamopleura miles (Carpenter in Pilsbry, 1893)South Andaman, IndiaOM758205Present study
Squamopleura miles (Carpenter in Pilsbry, 1893)South Andaman, IndiaOM758206Present study
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Alnashiri, H.; Thomas, L.; Thaikkottathil, M.; Philip, S.; Kutty, R.; Sivanpillai, S.; Abo Rasain, A.M. Phylogenetic Affinities of Acanthopleurinae Dall, 1889 Chitons (Mollusca: Polyplacophora: Chitonidae) from Jazan Coast in the Red Sea and Western Indo-Pacific. J. Mar. Sci. Eng. 2023, 11, 158. https://doi.org/10.3390/jmse11010158

AMA Style

Alnashiri H, Thomas L, Thaikkottathil M, Philip S, Kutty R, Sivanpillai S, Abo Rasain AM. Phylogenetic Affinities of Acanthopleurinae Dall, 1889 Chitons (Mollusca: Polyplacophora: Chitonidae) from Jazan Coast in the Red Sea and Western Indo-Pacific. Journal of Marine Science and Engineering. 2023; 11(1):158. https://doi.org/10.3390/jmse11010158

Chicago/Turabian Style

Alnashiri, Hassien, Liju Thomas, Maqbool Thaikkottathil, Siby Philip, Ranjeet Kutty, Sureshkumar Sivanpillai, and Ali Mohammed Abo Rasain. 2023. "Phylogenetic Affinities of Acanthopleurinae Dall, 1889 Chitons (Mollusca: Polyplacophora: Chitonidae) from Jazan Coast in the Red Sea and Western Indo-Pacific" Journal of Marine Science and Engineering 11, no. 1: 158. https://doi.org/10.3390/jmse11010158

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop