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An integrative framework to reevaluate the Neotropical catfish genus Guyanancistrus (Siluriformes: Loricariidae) with particular emphasis on the Guyanancistrus brevispinis complex
An integrative framework to reevaluate the Neotropical catfish genus Guyanancistrus (Siluriformes: Loricariidae) with particular emphasis on the Guyanancistrus brevispinis complex
Characterizing and naming species becomes more and more challenging due to the increasing difficulty of accurately delineating specific bounderies. In this context, integrative taxonomy aims to delimit taxonomic units by leveraging the complementarity of multiple data sources (geography, morphology, genetics, etc.). However, while the theoretical framework of integrative taxonomy has been explicitly stated, methods for the simultaneous analysis of multiple data sets are poorly developed and in many cases different information sources are still explored successively. Multi-table methods developed in the field of community ecology provide such an intregrative framework. In particular, multiple co-inertia analysis is flexible enough to allow the integration of morphological, distributional, and genetic data in the same analysis. We have applied this powerfull approach to delimit species boundaries in a group of poorly differentiated catfishes belonging to the genus Guyanancistrus from the Guianas region of northeastern South America. Because the species G. brevispinis has been claimed to be a species complex consisting of five species, particular attention was paid to taxon. Separate analyses indicated the presence of eight distinct species of Guyanancistrus, including five new species and one new genus. However, none of the preliminary analyses revealed different lineages within G. brevispinis, and the multi-table analysis revealed three intraspecific lineages. After taxonomic clarifications and description of the new genus, species and subspecies, a reappraisal of the biogeography of Guyanancistrus members was performed. This analysis revealed three distinct dispersals from the Upper reaches of Amazonian tributaries toward coastal rivers of the Eastern Guianas Ecoregion. The central role played by the Maroni River, as gateway from the Amazon basin, was confirmed. The Maroni River was also found to be a center of speciation for Guyanancistrus (with three species and two subspecies), as well as a source of dispersal of G. brevispinis toward the other main basins of the Eastern Guianas.
Citation: Fisch-Muller S, Mol JHA, Covain R (2018) An integrative framework to reevaluate the Neotropical catfish genus Guyanancistrus (Siluriformes: Loricariidae) with particular emphasis on the Guyanancistrus brevispinis complex. PLoS ONE 13(1): e0189789. https://doi.org/10.1371/journal.pone.0189789
Editor: Zuogang Peng, SOUTHWEST UNIVERSITY, CHINA
Received: May 12, 2017; Accepted: December 3, 2017; Published: January 3, 2018
Data Availability: All sequences and specimens data are available from the GenBank and BOLD databases (accession numbers provided in Table 1). All other relevant data are included within the paper and its Supporting Information files.
Funding: For their financial support, we acknowledge the Georges and Antoine Claraz Foundation for field missions in Suriname in 2001 and 2008, and in French Guiana in 2006; the Académie Suisse des Sciences Naturelles (ScNat) for the mission in French Guiana 2006; the Constantin Topali Found for the acquisition of lab material in 2009; the Département de la Culture et du Sport for the mission in Suriname in 2014. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Introduction
Species identification, characterization, and naming remain fundamental and critical steps in biological science. Since the establishment of the Linnean system [1], species have been described mainly on the basis of morphological and phenotypic characteristics. Through time, however, morphology alone has been shown to be limited in its ability to delineate species boundaries, and led to a proliferation of names and nomenclatural instability [2]. In addition, cryptic diversity (reviewed in [3]) remained hidden from traditional morphological approaches (see e.g. [4, 5]). Modern technological developments, including DNA sequencing, provide new tools allowing the detection of hidden diversity. In particular, the DNA barcoding approach [6], quickly appeared to be an efficient methodology for detecting cryptic biodiversity (e.g. [7–15]), even though in certain cases, such as recent divergence [16, 17] or mitochondrial introgression [18], barcoding may fail to discriminate between species (e.g. [19, 20]). Morphological data (used in systematics) and molecular data such as DNA barcodes (used in biodiversity studies) are not mutually exlusive, and often are complementary means of delineating species. Indeed, combining multiple data sources is the most efficient way to support robust species hypotheses [21–23]. Formalized under the designation “integrative taxonomy” [2, 24] (reviewed in [25, 26]), this approach tries to use the complementarity of the different fields of study (e.g. morphology, genetics, biogeography, ecology, ethology, etc.) to delineate, describe and name species. Various protocols have been proposed to integrate these different data sources [2, 25–27], but most of them correspond to guidelines that explore the different datasets successively to corroborate taxonomic hypotheses, or only focus on a given type of data (e.g. [28]). The way that results of the different analyses are interpreted, i.e. in a cumulative or a congruent way [25], also has an impact on the results, leading to an over-estimation of the number of species and lower confidence in species identity in the former case, and to an underestimation of the number of species and higher confidendence in species identity in the latter. Moreover, comparing results of different analyses, which can be based on qualitatively different data (e.g. linear measurements for morphometric analyses, sequence alignments for phylogenetic trees or distances matrices, GPS coordinates for distributional data, etc.), in the same descriptive framework remains a challenge.
Community ecologists, confronted by the same issue of combined analysis of various data types, developed multi-table methods (e.g. [29–34]). Based on the co-inertia criterion [29], multi-table analyses look for common structures present in different data sets, and include them in a common analysis. The link between all tables is defined by row, since all different observations (e.g. the abundances, the distributions, the life traits, etc.) rely on the same statistical units (e.g. the specimens, the stations, etc.). These analyses are particularly flexible and allow the inclusion of multiple data types, and have already been used in different fields including e.g. ecology, medical research, agronomy, evolutionary biology, and genomics [19, 29, 31, 35–40]. In addition, these methods allow evaluation of the statistical significance of the congruence between data types and the amount of common information present in the different tables. We consider the integrative approach of multi-table methods highly appropriate for the resolution of species delineation in a group of poorly-differentiated catfishes from the Guianese Region.
The northeastern part of the Guiana Shield, including Suriname and French Guiana, overlaps the Eastern Guianas Neotropical freshwater ecoregion [41]. This region ranges between the Demerara River in the west and the Oyapock River in the east and probably supports more than 500 described species, of which 169 are considered endemic (freshwater ecoregions of the world: http://www.feow.org/ecoregions/details/311, accessed 31th Jan. 2017), making the Eastern Guianas a region of high biodiversity importance [42, 43]. The Eastern Guianas’ river system comprises about a dozen important catchments, including, from west to east, the Corantijn, Nickerie, Coppename, Saramacca, Suriname, Maroni (= Marowijne in Suriname), Mana, Sinnamary, Comté-Orapu, Approuague, and Oyapock rivers. All these catchments are independant and flow from south to north into the Atlantic, making the Eastern Guianas rather isolated from the rest of the Guiana Shield, out of the direct influence of the Amazon and Orinoco basins. Le Bail et al. [44] listed 416 species of freshwater and estuarine fishes in French Guiana and Mol et al. [45] 481 freshwater fish species in Suriname. Among this tremendous diversity, the Characiformes was the most important group, representing about 40% of all species, followed by the Silurifomes at around 35%. Among the latter, the Loricariidae is the most diversified catfish family with more than 80 species distributed in French Guiana and Suriname.
The Loricariidae is a strictly Neotropical catfish family comprising 937 valid species and an estimated 300 undescribed species distributed in more than 100 genera [46–48], making it the most species rich family of the Siluriformes. Loricariids are primarily characterized by a depressed body covered by bony plates, and by an important modification of the mouth into a sucker disk. Among Loricariidae, the subfamily Hypostominae represents half of the familial diversity, comprising 465 valid species [48] distributed in more than 40 valid genera [49]. In French Guiana and Suriname nine genera are recorded [44, 45], including hyperendemic and monotypic representatives such as Hemiancistrus medians or Pseudoqolus koko [20, 50, 51], both restricted to the Maroni Basin. The other genera are more widely distributed in South America, with the exception of Guyanancistrus, restricted to the northeastern part of the Guiana Shield.
Isbrücker [52] described the genus Guyanancistrus, designating Lasiancistrus brevispinis Heitmans, Nijssen & Isbrücker 1983, a species present in Suriname and French Guiana, as the type species. Guyanancistrus was originally diagnosed on the basis of its similarity to Lasiancistrus Regan 1904 while differing from the latter in the absence of the characteristic bristles, or whisker-like odontodes, that are found among the hypertrophied odontodes on their evertible cheek plates. Guyanancistrus was placed in the synonymy of Pseudancistrus Bleecker 1962 by Armbruster [53, 54], based on a phylogenetic analysis of morphological characters that included most of the genera then placed in the subfamilies Hypostominae and Ancistrinae. However, a molecular phylogenetic analysis of the group using mitochondrial and nuclear sequence data revealed Pseudancistrus sensu lato to be a paraphyletic assemblage of five unrelated lineages [50]. One of the lineages uncovered corresponded to the genus Guyanancistrus. As well as G. brevispinis, two other species were included in the genus: G. niger (Norman 1926) and G. longispinis (Heitmans, Nijssen & Isbrücker 1983), both described from French Guiana and restricted to the Oyapock River Basin [44]. Additionally, a possibly new dwarf species collected in mountain streams flowing to the Marowijne River in Suriname was placed as a member of Guyanancistrus, and constituted the sister species of G. brevispinis [50]. This small species (<6 cm) nicknamed Bigmouth due to its particular morphology [55] was already suspected to be new by Mol [56] who collected it during a Rapid Assessment Program (RAP) survey to the Nassau Mountains. This revealed a highly endemic fauna now threatened with extinction by a bauxite mining project and illegal gold mining [19, 45, 57].
Unlike its congeners, Guyanancistrus brevispinis is known to be widespread, common and abundant, its area of distribution covering all the main Guianese river systems of Suriname and French Guiana, from the Corantijn in the west to the Oyapock in the east [44, 55, 58, 59]. Cardoso and Montoya-Burgos [60] analysed the species based on several of its populations, including Amazonian ones (from northern tributaries of the Paru de Oeste and Jari rivers), in order to decipher its historical biogeography, and found that it was genetically highly diversified, with six distinct allopatric lineages (five Guianese and one Amazonian). It was thus considered as a species complex, with the true G. brevispinis possibly restricted to the Nickerie River system (see [55]). However, additional sources of information from genetic markers were deemed necessary to confirm their taxonomic status. The five Atlantic coastal G. brevispinis lineages of the Guianas were found to form a monophyletic group that originated from an ancestral colonization event from the Amazonian Basin, hypothesized to have been through river capture between northern Amazon tributaries and the upper Maroni River Basin. In the Guianas, subsequent dispersal would mainly have resulted from temporary connections between adjacent rivers when sea levels were low, and subsequent diversification of isolated populations during periods with high sea levels [60].
Considering the recent genus revalidation and questions about the type species, and the potential existence of new and/or endangered species, the present work uses an integrative approach combining morphology, genetics and spatial data to reappraise Guyanancistrus, focusing on the enigmatic Guyanancistrus brevispinis species complex. Most known populations were included in this analysis, principally based on material collected by the authors and their collaborators in the past 15 years. After a comparative diagnosis of the genus, the type species is redefined and its morphological and genetic variation delineated. Several new species revealed by the study are also described. Detailed descriptions and morphological comparisons of Guyanancistrus niger and G. longispinis are already available [59, 61, 62] and will not be repeated, but a practical key to all Guyanancistrus species is provided. After this taxonomic clarification, the biogeography of all Guyanancistrus members is re-evaluated to investigate dispersal processes, putative local extinctions, and speciation events.