Speciation in Ancient Cryptic Species Complexes: Evidence From the Molecular Phylogeny of Brachionus Plicatilis (Rotifera)

Abstract

Continental lake-dwelling zooplanktonic organisms have long been considered cosmopolitan species with little geographic variation in spite of the isolation of their habitats. Evidence of morphological cohesiveness and high dispersal capabilities support this interpretation. However, this view has been challenged recently as many such species have been shown either to comprise cryptic species complexes or to exhibit marked population genetic differentiation and strong phylogeographic structuring at a regional scale. Here we investigate the molecular phylogeny of the cosmopolitan passively dispersing rotifer Brachionus plicatilis (Rotifera: Monogononta) species complex using nucleotide sequence variation from both nuclear (ribosomal internal transcribed spacer 1, ITS1) and mitochondrial (cytochrome c oxidase subunit I, COI) genes. Analysis of rotifer resting eggs from 27 salt lakes in the Iberian Peninsula plus lakes from four continents revealed nine genetically divergent lineages. The high level of sequence divergence, absence of hybridization, and extensive sympatry observed support the specific status of these lineages. Sequence divergence estimates indicate that the B. plicatilis complex began diversifying many millions of years ago, yet has showed relatively high levels of morphological stasis. We discuss these results in relation to the ecology and genetics of aquatic invertebrates possessing dispersive resting propagules and address the apparent contradiction between zooplanktonic population structure and their morphological stasis.

Updating the description and taxonomic status of Brachionus sessilis Varga, 1951 (Rotifera: Brachionidae) based on detailed morphological analysis and molecular data

“…Cayman and B. plicatilis were found to comprise more than a single species in concordance with previous reports (e.g. Gómez et al 2002;Suatoni et al 2006). …”

“…As a consequence, markedly different morphological variants can be found within the same species (Ahlstrom 1940). On the other hand, remarkable interspecific similarity also exists as in the case of the B. plicatilis complex of cryptic species in which several morphologically similar albeit phylogenetically distinct lineages have been identified (Gómez et al 2002;Suatoni et al 2006). These characteristics, along with other taxonomic difficulties typical of the phylum, such as the dearth of taxonomically important morphological characters (Ahlstrom 1940), the deficiency of comprehensive descriptions including analysis of biometry or geometric morphometrics (Koste & Shiel 1989;Adams et al 2004), the improper use of infraspecific rank names and a long list of synonyms (Harring 1913;Segers 2007) pose major taxonomic impediments to the taxonomists dealing with the systematics of Brachionus rotifers.…”

Native, alien, cosmopolitan, or cryptogenic? A framework for clarifying the origin status of rotifers

“…The level of rotifer diversity revealed by DNA studies may be significantly higher than that calculated on the basis of traditional taxonomy. For example, the apparent cosmopolitanism in the monogonont Brachionus plicatilis is actually due to the fact that it comprises a cryptic species complex, with as many as 22 morphologically similar taxa having more restricted distributions (Gómez et al 2002). Moreover, a complex of at least 24 taxa was found in the British bdelloid Rotatoria rotatoria (Fontaneto et al 2009).…”

“…On the one hand, these findings suggest that the level of endemism among microorganisms may be higher than previously thought, which increases the probability of human intervention in the case of widely distributed species. However, some of the taxa distinguished from cryptic species complexes indeed have a very wide distribution (Gómez et al 2002). Successful colonization of such vast areas seems relatively recent from an evolutionary time perspective, and it is usually attributed to the high capabilities of microorganisms for long-distance passive dispersal by natural vectors (Cáceres & Soluk 2002, Gómez et al 2002, Green & Figuerola 2005, Incagnone et al 2015.…”

“…We use rotifers recorded in Europe as an example. The biogeography of this group has recently received considerable attention (Gómez et al 2002, Fontaneto et al 2007, Schröder & Walsh 2007, although the problem of their origin status has rarely been addressed. Traditionally, rotifers were considered cosmopolitan, fitting the concept of ubiquitous species (Pejler 1977, Ruttner-Kolisko 1989, Artois et al 2011, despite attempts by Green (1972) to bring some subtlety into the picture by classifying rotifers into cosmopolitan, cosmotropical, tropicopolitan, or Arctic-temperate species.…”