A cornucopia of cryptic species - a DNA barcode analysis of the gobiid fish genus Trimma (Percomorpha, Gobiiformes)

Abstract

A genetic analysis of partial mitochondrial 5’ cytochrome c oxidase I gene (DNA barcode) sequences of 473 specimens assigned to 52 morphological species (including four known, but not formally named, species) of the gobiid genus Trimma revealed the presence of 94 genetic lineages. Each lineage was separated by > 2% sequence divergence. Thus there were an additional 42 haplogroups recognizable as provisional candidate species given that a value of > 2% difference is typical of different species of fishes. Such a high degree of apparently different cryptic species is, in our experience, virtually unprecedented among vertebrates. These results have precipitated further morphological research in a few cases, which has uncovered subtle differences independently corroborating the genetic results. However, such efforts are limited by the dearth of traditional systematists available to undertake the necessary time-consuming, and highly detailed, morphological research. In some cases, the genetic results we present are consistent with, and confirm, minor taxonomic distinctions based on morphology and/or colour pattern. In other instances, what had been recognized as a single species consists of several genetic lineages - up to eight in, for example, what we have identified based on morphology as Trimma okinawae. The increase from 52 to 94 potential species in our sampling raises the predicted total number of species in this genus from about 110 to nearly 200 (versus the 73 valid described species currently recognized).

DNA barcodes for ecology, evolution, and conservation

“…An extensive DNA barcode study on Microgastrinae wasps demonstrated significant insights into their taxonomy and species discovery [22]. Such cryptic diversity has been uncovered using DNA barcodes in other animal taxa, including crustaceans, diatoms, and fish [23][24][25]. The use of DNA barcodes for the discovery of new species is emerging as a powerful tool to clarify species boundaries and to quantify species diversity [26].…”

“…DNA barcodes in conjunction with morphological, biochemical, and ecological information are revealing an outstanding diversity of species previously unrecognized through the analysis of morphological variation alone. During the first 8 months of 2014, the Web of Science recorded 310 publications in which DNA barcoding was used in discovering and describing new species, including algae [78], ferns [79], fungi [80], nematodes [81,82], arthropods [83,84], mollusks [85], fish [25], birds [86], and mammals [87]. Early on, it was expected that a single genetic marker would serve as a universal DNA barcode to identify species across the eukaryotic Tree of Life.…”

DNA barcoding the ichthyofauna of the Yangtze River: Insights from the molecular inventory of a mega‐diverse temperate fauna

“…Initially designed to conduct individual identifications to the species level (Hubert & Hanner, ), this approach also proved to be helpful in performing a preliminary assessment of extremely diverse and poorly known fauna awaiting species delimitation (Janzen, Hajibabaei, & Burns, ; Riedel, Sagata, Suhardjono, Tänzler, & Balke, ; Smith, Fisher, & Hebert, ; Smith, Rodriguez, & Whitfield, ; Smith, Wood, Janzen, Hallwachs, & Hebert, ; Tänzler, Sagata, Surbakti, Balke, & Riedel, ). Recent large‐scale assessments of diverse ichthyofauna confirmed that the use of the cytochrome oxidase I gene successfully capture a large portion of the alpha diversity for well‐known fauna (April, Mayden, Hanner, & Bernatchez, ; Hubert, Hanner, & Holm, ; Ward, Zemlak, Innes, Last, & Hebert, ) but also helped in highlighting unrecognized (i.e., cryptic) diversity (Durand, Hubert, Shen, & Borsa, ; Hubert, Meyer, & Bruggemann, ; Jaafar, Taylor, Mohd Nor, Bruyn, & Carvalho, ; Pereira, Pazian, Hanner, Foresti, & Oliveira, ; Rock, Costa, & Walker, ; Winterbottom, Hanner, Burridge, & Zur, ). Landscape features such as fragmentation, however, proved to be a challenge to accurately delimit species through DNA barcodes (Geiger, Herder, & Monaghan, ; Keskin, Agdamar, & Tarkan, ; Knebelsberger, Dunz, Neumann, & Geiger, ).…”

Geography and life history traits account for the accumulation of cryptic diversity among Indo-West Pacific coral reef fishes

“…ocean basin) to local (i.e. island) scales (Hubert et al 2012, Winterbottom et al 2014, Tornabene et al 2015. Unacknowledged cryptic diversity in Indo-West Pacific reef fish communities hampers our understanding of diversity patterns (Leprieur et al 2012, Mouillot et al 2013, Pellissier et al 2014) and their origin (McCafferty et al 2002, Kuriiwa et al 2007, Drew & Barber 2009, Leray et al 2010, Winters et al 2010, Gaither et al 2011, Borsa et al 2013, Sims et al 2014, Durand & Borsa 2015, Tornabene et al 2015.…”

“…A broad assessment of the factors promoting cryptic diversity in coral reef ecosystems is timely, because the exploration of diversity patterns in the Indo-West Pacific is an increasingly debated topic (Jokiel & Martinelli 1992, Briggs 1999, Halas & Winterbottom 2009, Hubert et al 2012, Gaither & Rocha 2013, Tornabene et al 2015. The conservation of coral reefs also requires up-todate checklists of species whose accuracy depends on the approach involved in species delineation (Hubert et al 2012, Winterbottom et al 2014, Pante et al 2015, Tornabene et al 2015.…”