Effects of phylogenetic reconstruction method on the robustness of species delimitation using single-locus data

1. Coalescent-based species delimitation methods combine population genetic and phylogenetic theory to provide an objective means for delineating evolutionarily significant units of diversity. The Generalized Mixed Yule Coalescent (GMYC) and the Poisson Tree Process (PTP) are methods that use ultrametric (GMYC or PTP) or non-ultrametric (PTP) gene trees as input, intended for use mostly with single-locus data such as DNA barcodes. 2. Here we assess how robust the GMYC and PTP are to different phylogenetic reconstruction and branch smoothing methods. We reconstruct over 400 ultrametric trees using up to 30 different combinations of phylogenetic and smoothing methods and perform over 2,000 separate species delimitation analyses across 16 empirical datasets. We then assess how variable diversity estimates are, in terms of richness and identity, with respect to species delimitation, phylogenetic and smoothing methods. 3. The PTP method generally generates diversity estimates that are more robust to different phylogenetic methods. The GMYC is more sensitive, but provides consistent estimates for BEAST trees. The lower consistency of GMYC estimates is likely a result of differences among gene trees introduced by the smoothing step. Unresolved nodes (real anomalies or methodological artefacts) affect both GMYC and PTP estimates, but have a greater effect on GMYC estimates. Branch smoothing is a difficult step and perhaps an underappreciated source of bias that may be widespread among studies of diversity and diversification. 4. Nevertheless, careful choice of phylogenetic method does produce equivalent PTP and GMYC diversity estimates. We recommend simultaneous use of the PTP model with any model-based gene tree (e.g. RAxML) and GMYC approaches with BEAST trees for obtaining species hypotheses

Cryptic diversity of Synchaeta spp. (Rotifera, Monogononta) in mountain lakes: relationships with environmental parameters

Cryptic species (i.e. distinct species that are morphologically similar) may have different ecological requirements and their merging into one species can bias the assessment of the main ecological drivers of biodiversity. We investigated the environmental parameters influencing the occurrence of Synchaeta species (S. pectinata, S. grandis, S. lakowitziana, S. tremula/oblonga - monogonont rotifers) in 17 waterbodies of the Trentino-South Tyrol region in the Eastern Alps. To improve taxonomic resolution in phylogenetic analysis, a marine Synchaeta (i.e. S. cf. cecilia) from the United Kingdom was also sampled and sequences from GenBank were downloaded. While Synchaeta species were morphologically identified based on trophi structure, cryptic species were identified based on the generalised mixed Yule coalescent (GMYC) model. We performed multivariate ordination both for morphospecies (i.e. unresolved complexes of cryptic species), a common practice in limnological studies based on morphological taxonomy, and for putative cryptic species, made possible by DNA taxonomy. We expected that resolving complexes of cryptic species could provide more information than using morphospecies. Out of the overall phylogenetic tree with 48 haplotypes from 203 individuals, the GMYC model indicated the presence of 14 GMYC entities, 11 from lakes in the Eastern Alps, 2 from Canada, and one from the U.K. Synchaeta pectinata showed five GMYC entities and S. tremula showed two; all individuals, for which the identification to S. tremula or S. oblonga was not possible, clustered in one monophyletic clade, here called S. tremula/oblonga, that showed additional evidence of three GMYC entities. Environmental-based multivariate ordination on cryptic species explained a significantly higher proportion of variance than that based on morphospecies. Occurrence of putative cryptic species was mainly related to total phosphorus. Moreover, different cryptic species within the same morphospecies showed different, and even opposite, preferences for total phosphorus. In addition, the same GMYC entity of S. tremula/oblonga found in Trentino-South Tyrol was also present in Canada and the same haplotype of S. pectinata found in Trentino-South Tyrol was also found in the U.K. This wide geographical distribution of haplotypes and cryptic species indicated the absence of dispersal barriers in Synchaet

Sexual species are separated by larger genetic gaps than asexual species in rotifers.

Why organisms diversify into discrete species instead of showing a continuum of genotypic and phenotypic forms is an important yet rarely studied question in speciation biology. Does species discreteness come from adaptation to fill discrete niches or from interspecific gaps generated by reproductive isolation? We investigate the importance of reproductive isolation by comparing genetic discreteness, in terms of intra- and interspecific variation, between facultatively sexual monogonont rotifers and obligately asexual bdelloid rotifers. We calculated the age (phylogenetic distance) and average pairwise genetic distance (raw distance) within and among evolutionarily significant units of diversity in six bdelloid clades and seven monogonont clades sampled for 4211 individuals in total. We find that monogonont species are more discrete than bdelloid species with respect to divergence between species but exhibit similar levels of intraspecific variation (species cohesiveness). This pattern arises because bdelloids have diversified into discrete genetic clusters at a faster net rate than monogononts. Although sampling biases or differences in ecology that are independent of sexuality might also affect these patterns, the results are consistent with the hypothesis that bdelloids diversified at a faster rate into less discrete species because their diversification does not depend on the evolution of reproductive isolation

Is the human population a large-scale indicator of the species richness of ground beetles?

Aim Positive regional correlations between biodiversity and human population have been detected for several taxonomic groups and geographical regions. Such correlations could have important conservation implications and have been mainly attributed to ecological factors, with little testing for an artefactual explanation: more populated regions may show higher biodiversity because they are more thoroughly surveyed. We tested the hypothesis that the correlation between people and herptile diversity in Europe is influenced by survey effor

Positive regional species-people correlations: A sampling artefact or a key issue for sustainable development?

Many studies are documenting positive large-scale species– people correlations (Luck, 2007; Schuldt & Assmann, 2010). The issue is scale dependent: the local association of species richness and people is in many cases a negative one (Pautasso, 2007; Pecher et al., 2010). This biogeographical pattern is thus important for conservation. If species-rich regions are also densely populated, preserving biodiversity becomes more difficult, ceteris paribus, than if species-rich regions were sparsely populated. At the same time, positive, regional species–people correlations are an opportunity for the biodiversity education of the majority of the human population and underline the importance of conservation in human-modified landscapes (e.g. Sheil & Meijaard, 2010; Ward, 2010)

The 'rotiferologist' effect and other global correlates of species richness in monogonont rotifers

Global biodiversity patterns are often driven by diff erent environmental variables at diff erent scales. However, it is still controversial whether there are general trends, whether similar processes are responsible for similar patterns, and/or whether confounding eff ects such as sampling bias can produce misleading results. Our aim is twofold: 1) assessing the global correlates of diversity in a group of microscopic animals little analysed so far, and 2) inferring the infl uence of sampling intensity on biodiversity analyses. As a case study, we choose rotifers, because of their high potential for dispersal across the globe. We assembled and analysed a new worldwide dataset of records of monogonont rotifers, a group of microscopic aquatic animals, from 1960 to 1992. Using spatially explicit models, we assessed whether the diversity patterns conformed to those commonly obtained for larger organisms, and whether they still held true after controlling for sampling intensity, variations in area, and spatial structure in the data. Our results are in part analogous to those commonly obtained for macroorganisms (habitat heterogeneity and precipitation emerge as the main global correlates), but show some divergence (potential absence of a latitudinal gradient and of a large-scale correlation with human population). Moreover, the eff ect of sampling eff ort is remarkable, accounting for 50% of the variability; this strong eff ect may mask other patterns such as latitudinal gradients. Our study points out that sampling bias should be carefully considered when drawing conclusions from large-scale analyses, and calls for further faunistic work on microorganisms in all regions of the world to better understand the generality of the processes driving global patterns in biodiversity

Evidence of Weak Habitat Specialisation in Microscopic Animals

Macroecology and biogeography of microscopic organisms (any living organism smaller than 2 mm) are quickly developing into fruitful research areas. Microscopic organisms also offer the potential for testing predictions and models derived from observations on larger organisms due to the feasibility of performing lab and mesocosm experiments. However, more empirical knowledge on the similarities and differences between micro- and macro-organisms is needed to ascertain how much of the results obtained from the former can be generalised to the latter. One potential misconception, based mostly on anedoctal evidence rather than explicit tests, is that microscopic organisms may have wider ecological tolerance and a lower degree of habitat specialisation than large organisms. Here we explicitly test this hypothesis within the framework of metacommunity theory, by studying host specificify in the assemblages of bdelloid rotifers (animals about 350 µm in body length) living in different species of lichens in Sweden. Using several regression-based and ANOVA analyses and controlling for both spatial structure and the kind of substrate the lichen grow over (bark vs rock), we found evidence of significant but weak species-specific associations between bdelloids and lichens, a wide overlap in species composition between lichens, and wide ecological tolerance for most bdelloid species. This confirms that microscopic organisms such as bdelloids have a lower degree of habitat specialisation than larger organisms, although this happens in a complex scenario of ecological processes, where source-sink dynamics and geographic distances seem to have no effect on species composition at the analysed scale

Horizontal gene transfer in bdelloid rotifers is ancient, ongoing and more frequent in species from desiccating habitats.

BACKGROUND: Although prevalent in prokaryotes, horizontal gene transfer (HGT) is rarer in multicellular eukaryotes. Bdelloid rotifers are microscopic animals that contain a higher proportion of horizontally transferred, non-metazoan genes in their genomes than typical of animals. It has been hypothesized that bdelloids incorporate foreign DNA when they repair their chromosomes following double-strand breaks caused by desiccation. HGT might thereby contribute to species divergence and adaptation, as in prokaryotes. If so, we expect that species should differ in their complement of foreign genes, rather than sharing the same set of foreign genes inherited from a common ancestor. Furthermore, there should be more foreign genes in species that desiccate more frequently. We tested these hypotheses by surveying HGT in four congeneric species of bdelloids from different habitats: two from permanent aquatic habitats and two from temporary aquatic habitats that desiccate regularly. RESULTS: Transcriptomes of all four species contain many genes with a closer match to non-metazoan genes than to metazoan genes. Whole genome sequencing of one species confirmed the presence of these foreign genes in the genome. Nearly half of foreign genes are shared between all four species and an outgroup from another family, but many hundreds are unique to particular species, which indicates that HGT is ongoing. Using a dated phylogeny, we estimate an average of 12.8 gains versus 2.0 losses of foreign genes per million years. Consistent with the desiccation hypothesis, the level of HGT is higher in the species that experience regular desiccation events than those that do not. However, HGT still contributed hundreds of foreign genes to the species from permanently aquatic habitats. Foreign genes were mainly enzymes with various annotated functions that include catabolism of complex polysaccharides and stress responses. We found evidence of differential loss of ancestral foreign genes previously associated with desiccation protection in the two non-desiccating species. CONCLUSIONS: Nearly half of foreign genes were acquired before the divergence of bdelloid families over 60 Mya. Nonetheless, HGT is ongoing in bdelloids and has contributed to putative functional differences among species. Variation among our study species is consistent with the hypothesis that desiccating habitats promote HGT

Identification key to the genera of marine rotifers worldwide

A dichotomous key to rotifers is presented for the 28 Families and 66 Genera that have been reported from saline systems of both marine and inland waters. Information is provided on general identification and papers dealing more particularly with certain Families and Genera. A succinct overview of the species found in saline habitats is given for each genus

Towards a list of available names in zoology, partim Phylum Rotifera

Many, mostly older, names of animal species are nomenclaturally problematic, either because their orthography is unstable, or they cannot be linked reliably to a taxonomic identity, due to the lack of recognisable descriptions and/or types. Yet, they represent available (sensu International Code of Zoological Nomenclature) names and must be taken into account in zoological works. This situation, with available senior, yet dubious names confounding nomenclature, is undesirable. It creates uncertainties at a time when molecular approaches are revolutionizing our concepts of species diversity, and fails us when the current extinction crisis calls for efficient, accurate, and constructive approaches to document, monitor, and conserve biodiversity. The International Code of Zoological Nomenclature (The Code) provides a means to address this issue by restricting availability, application and orthography of names to those included in the List of Available Names in Zoology (LAN). The Code (Art. 79) allows an international body of zoologists in consultation with the Commission to propose a candidate part of the LAN for a major taxonomic field. We explore this possibility for 3570 species-group names of Phylum Rotifera (of which 665 are problematic), by presenting such a candidate Rotifera part of the LAN. The web site of the International Commission on Zoological Nomenclature (http://www.iczn.org) will hold both the candidate list and a forum to facilitate consultation on the candidate list, while the list itself also can already be freely downloaded from three other Internet sites: http://fada.biodiversity. be, http://rotifer.ansp.org/LAN, and www.hausdernatur.at/rotifera. We give here an overview of the general approach and procedures applied in preparation of the candidate list, and anticipate that our effort will promote the process as well as result in a standard list of names for use in taxonomy, the Global Names Architecture and other biodiversity information initiatives