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Remarks on Mastigodiaptomus (Calanoida: Diaptomidae) from Mexico Using Integrative Taxonomy, with a Key of Identification and Three New Species

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Remarks on Mastigodiaptomus (Calanoida: Diaptomidae) from Mexico Using Integrative Taxonomy, with a Key of Identification and Three New Species Remarks on Mastigodiaptomus (Calanoida: Diaptomidae) from Mexico using integrative taxonomy, with a key of identification and three new species Martha A. Gutiérrez-Aguirre1, Adrián Cervantes-Martínez1, Manuel Elías-Gutiérrez2 and Alfonso Lugo-Vázquez3 1 Departamento de Ciencias y Humanidades, Universidad de Quintana Roo, Cozumel, Quintana Roo, Mexico 2 Departamento de Sistemática y Ecología Acuática, El Colegio de la Frontera Sur, Chetumal, Quintana Roo, Mexico 3 Unidad de Investigación Interdisciplinaria en Ciencias de la Salud y la Educación, Universidad Nacional Autónoma de México, Los Reyes Iztacala, Tlalnepantla, Estado de México, Mexico ABSTRACT Background: In Mexico, species of four families of free-living calanoid copepods have been recorded as inhabitants of several freshwater systems. These families are Centropagidae, Temoridae, Pseudodiaptomidae and Diaptomidae. The genera Leptodiaptomus and Mastigodiaptomus are the most speciose diaptomid genera in Mexico, and they inhabit natural and artificial lakes, ephemeral ponds, springs, and caverns. Leptodiaptomus is considered as an endemic Nearctic genus, whereas Mastigodiaptomus is a widely distributed Neotropical genus in the southern USA, Mexico, the Caribbean Islands and Central America. Based on new and recent evidence, Mastigodiaptomus diversity has been underestimated: six species of the genus were known before 2000. In this work three new Mastigodiaptomus species have been described from different regions of Mexico by using integrative taxonomy. We also gave amended diagnosis of M. nesus Bowman (1986) and M. patzcuarensis s. str. (Kiefer, 1938). Submitted 27 September 2019 Methods: In this work, the taxonomic status of the species was clarified using Accepted 16 December 2019 Published 29 January 2020 modern, integrative method based on the COI gene as a DNA marker, plus micro-structural analysis (based on SEM and ligth microscopy). Corresponding author Martha A. Gutiérrez-Aguirre, Results: Three new species of Mastigodiaptomus were described based on genetic and [email protected] morphological analyses: M. alexei sp. n., M. ha sp. n. and M. cihuatlan sp. n. Also Academic editor amended description of M. nesus, morphological variation of M. patzcuarensis Hugo Sarmento s. str., and a comparison of them with all known sequences within the genus are Additional Information and provided. These new findings show that in Mastigodiaptomus differences in several Declarations can be found on cuticular microstructures of several appendages (such as the antennules, the fifth page 40 legs, or the urosomites of these copepods) agree with the interspecific genetic DOI 10.7717/peerj.8416 divergence >3% observed in sequences of the COI gene, and the integration of this Copyright information is a powerful tool in species delineation. 2020 Gutiérrez-Aguirre et al. Distributed under Creative Commons CC-BY 4.0 Subjects Biodiversity, Taxonomy, Freshwater Biology Keywords COI gene, Freshwater, Barcodes, Zooplankton, Copepoda, Neotropical How to cite this article Gutiérrez-Aguirre MA, Cervantes-Martínez A, Elías-Gutiérrez M, Lugo-Vázquez A. 2020. Remarks on Mastigodiaptomus (Calanoida: Diaptomidae) from Mexico using integrative taxonomy, with a key of identification and three new species. PeerJ 8:e8416 DOI 10.7717/peerj.8416 INTRODUCTION In Mexico, species of four families of free-living calanoid copepods have been recorded as inhabitants of several freshwater systems. These families are Centropagidae, Temoridae, Pseudodiaptomidae and Diaptomidae. The genera Leptodiaptomus and Mastigodiaptomus are the most speciose diaptomid genera in Mexico, and they inhabit natural and artificial lakes, ephemeral ponds, springs, and caverns. Leptodiaptomus is considered as an endemic Nearctic genus, whereas Mastigodiaptomus is a widely distributed Neotropical genus in the southern USA, Mexico, the Caribbean Islands and Central America. Based on new and recent evidence, Mastigodiaptomus diversity has been underestimated: six species of the genus were known before 2000 (Suárez-Morales & Elías-Gutiérrez, 2000). Recently, however, five new Mastigodiaptomus species have been described from different regions of Mexico by using integrative taxonomy (Suárez- Morales & Elías-Gutiérrez, 2000; Gutiérrez-Aguirre & Cervantes-Martínez, 2013; Gutiérrez-Aguirre, Cervantes-Martínez & Elías-Gutiérrez, 2014; Mercado-Salas et al., 2018). Under this assumption, in this paper, three new species of Mastigodiaptomus are described based on genetic and morphological analyses. In addition, amended description of Mastigodiaptomus nesus Bowman, 1986 and M. patzcuarensis (Kiefer, 1938) and a comparison of them with all known sequences within the genus is provided. Finally, a key (based on the morphology) for the identification of the known species of the genus is yielded. MATERIALS AND METHODS Morphological analysis Biological samples were obtained by limnetic plankton trawls using a plankton net with 50 mm mesh, and the material was fixed in 96% ethanol. The surveyed samples were collected along a latitudinal gradient from 17 to 24 N and a longitudinal gradient from 87 to 101 W. A full morphological description of adult males and females of the three new species, as well as an amended description of one more species of Mastigodiaptomus, is presented: the morphology of paratype specimens of M. nesus was analysed. Detailed analysis and illustration of morphology were performed with the aid of a camera lucida, light microscopy and the scanning electron microscopy JEOL-SM-6010, located at El Colegio de la Frontera Sur (ECOSUR, Chetumal Unit) according to Suárez-Morales et al. (1996). Several analysed specimens were dissected with tungsten needles, and their appendages were mounted in glycerine. The un-dissected biological material was preserved in 100% ethanol with a drop of glycerine. The type material and specimens were deposited in the Reference Collection at El Colegio de la Frontera Sur (ECOCH- CH-Z). Gutiérrez-Aguirre et al. (2020), PeerJ, DOI 10.7717/peerj.8416 2/43 The abbreviations for the appendages or anatomical micro-structure of the body of the adult females and males analysed here are based on those used by Huys & Boxshall (1991), Gutiérrez-Aguirre & Cervantes-Martínez (2016) and Mercado-Salas et al. (2018): A1 = antennule; Enp1–Enp3 = first to third endopodal segment; Exp1–Exp3 = first to third exopodal segment; P1–P5 = legs 1–5; Bsp = basipodite; s = setae; sp = spine; sps = spiniform process; ae = aesthetasc; ms = modified seta. DNA marker and extraction, PCR products and sequencing The COI gene, known as DNA barcode (Hebert et al., 2003), was here used as a marker to delimit the species as in previous studies (Gutiérrez-Aguirre, Cervantes-Martínez & Elías-Gutiérrez, 2014; Mercado-Salas et al., 2018). DNA was extracted using a standard glass fibre method (Ivanova, DeWaard & Hebert, 2006) from dorsal muscles of the cephalothorax or eggs (in egg-carrying females) following Elías-Gutiérrez et al. (2018). In all cases, the vouchers were deposited in the Reference Collection at El Colegio de la Frontera Sur, Unidad Chetumal (Access Numbers ECOCH-CH-Z-10312 to 10328). All sequences were uploaded to the Barcode of Life Database (BOLD, boldsystems.org) and GenBank (https://www.ncbi.nlm.nih.gov/genbank/). DNA extraction: 2 ml of each DNA extract was added to a PCR mixture consisting of 2 ml of HyClone ultra-pure water (Thermo Fisher Scientific, Waltham, MA, USA), 6.25 mlof 10% D-(+)-trehalose dihydrate (Fluka Analytical, Munich, Germany), 1.25 ml of 10× m m Platinum Taq buffer (Invitrogen, Carlsbad, CA, USA), 0.625 lof50 M MgCl2 (Invitrogen, Carlsbad, CA, USA), 0.0625 mlof10mM dNTP (KAPA Biosystems, Wilmington, MA, USA), 0.125 ml each of 10 mM Zplank primers (Prosser, Martínez-Arce & Elías-Gutiérrez, 2013), and 0.06 ml of PlatinumTaq (Invitrogen, Carlsbad, CA, USA). The reactions were cycled at 95 C for 1 min, followed by 5 cycles of (94 C for 40 s, 45 C for 40 s and 72 C for 1 min), 35 cycles of (94 C for 40 s, 51 C for 40 s and 72 C for 1 min), and a final extension of 72 C for 5 min. Products: PCR products were visualised on a 2% agarose gel using an E-Gel 95-well Pre-cast Agarose Electrophoresis System (Invitrogen, Carlsbad, CA, USA), and the detected PCR products were selected for sequencing. Products were labelled with a BigDye© Terminator v. 3.1 Cycle Sequencing Kit (Applied Biosystems, Inc., Foster City, CA, USA) and sequenced bidirectionally on an ABI 3730 capillary sequencer. Sequence data, trace files, collection data, and primer details for all specimens are available within the two project files in the Barcode of Life Data System (http://www.barcodinglife.org) and in GenBank. Bidirectional sequences were assembled and simultaneously aligned in SeqScape 2.1.1 (Applied Biosystems, Foster City, CA, USA). All sequences were searched against the BOLD (boldsystems.org). Sequences of closely related species were downloaded from the system and included in the analyses. With all sequences the public dataset with the name Mastigodiaptomus was created in BOLD database (DOI: 10.5883/DS-MMASTIGO). With the Alignment Transformation Environment (ALTER, http://www.sing-group. org/ALTER/), representative haplotypes of all the genetic variants of COI within and between species were obtained (Supplemental File 1). The FASTA files obtained were Gutiérrez-Aguirre et al. (2020), PeerJ, DOI 10.7717/peerj.8416 3/43 Table 1 Ornamentation of prosomal appendages. Armament of swimming legs (P1–P4) in the females and males of the Mastigodiaptomus species described here. Roman numerals indicate spines, and arabic numbers are setae. Coxa Basis Exp Enp P1 0-1 0-0 I-1; 0-1; I-3-2 0-1; 1-2-3 P2 0-1 0-0 I-1: I-1; I-3-3 0-1; 0-2; 2-2-3 P3 0-1 0-0 I-1; I-1; I-3-3 0-1; 0-2; 2-2-3 P4 0-1 1-0 I-1; I-1; I-3-3 0-1; 0-2; 2-2-3 then introduced into PGDSpider Vers. 2.1.1.5 (http://www.cmpg.unibe.ch/software/ PGDSpider/) to obtain the nexus file compatible with MrBayes Vers. 3.2.5 and jModelTest 2.1.10.
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