Delimiting species without monophyletic gene trees.
ABSTRACT Genetic data are frequently used to delimit species, where species status is determined on the basis of an exclusivity criterium, such as reciprocal monophyly. Not only are there numerous empirical examples of incongruence between the boundaries inferred from such data compared to other sources like morphology -- especially with recently derived species, but population genetic theory also clearly shows that an inevitable bias in species status results because genetic thresholds do not explicitly take into account how the timing of speciation influences patterns of genetic differentiation. This study represents a fundamental shift in how genetic data might be used to delimit species. Rather than equating gene trees with a species tree or basing species status on some genetic threshold, the relationship between the gene trees and the species history is modeled probabilistically. Here we show that the same theory that is used to calculate the probability of reciprocal monophyly can also be used to delimit species despite widespread incomplete lineage sorting. The results from a preliminary simulation study suggest that very recently derived species can be accurately identified long before the requisite time for reciprocal monophyly to be achieved following speciation. The study also indicates the importance of sampling, both with regards to loci and individuals. Withstanding a thorough investigation into the conditions under which the coalescent-based approach will be effective, namely how the timing of divergence relative to the effective population size of species affects accurate species delimitation, the results are nevertheless consistent with other recent studies (aimed at inferring species relationships), showing that despite the lack of monophyletic gene trees, a signal of species divergence persists and can be extracted. Using an explicit model-based approach also avoids two primary problems with species delimitation that result when genetic thresholds are applied with genetic data -- the inherent biases in species detection arising from when and how speciation occurred, and failure to take into account the high stochastic variance of genetic processes. Both the utility and sensitivities of the coalescent-based approach outlined here are discussed; most notably, a model-based approach is essential for determining whether incompletely sorted gene lineages are (or are not) consistent with separate species lineages, and such inferences require accurate model parameterization (i.e., a range of realistic effective population sizes relative to potential times of divergence for the purported species). It is the goal (and motivation of this study) that genetic data might be used effectively as a source of complementation to other sources of data for diagnosing species, as opposed to the exclusion of other evidence for species delimitation, which will require an explicit consideration of the effects of the temporal dynamic of lineage splitting on genetic data.
Article: Miocene and Pliocene dominated diversification of the lichen-forming fungal genus Melanohalea (Parmeliaceae, Ascomycota) and Pleistocene population expansions.[show abstract] [hide abstract]
ABSTRACT: BACKGROUND: Factors promoting diversification in lichen symbioses remain largely unexplored. While Pleistocene events have been important for driving diversification and affecting distributions in many groups, recent estimates suggest that major radiations within some genera in the largest clade of macrolichens (Parmeliaceae, Ascomycota) vastly predate the Pleistocene. To better understand the temporal placement and sequence of diversification events in lichens, we estimated divergence times in a common lichen-forming fungal genus, Melanohalea, in the Northern Hemisphere. Divergence times were estimated using both concatenated gene tree and coalescence-based multilocus species tree approaches to assess the temporal context of major radiation events within Melanohalea. In order to complement our understanding of processes impacting genetic differentiation, we also evaluated the effects of Pleistocene glacial cycles on population demographics of distinct Melanohalea lineages, differing in reproductive strategies. RESULTS: We found that divergence estimates, from both concatenated gene tree and coalescence-based multilocus species tree approaches, suggest that diversification within Melanohalea occurred predominantly during the Miocene and Pliocene, although estimated of divergence times differed by up to 8.3 million years between the two methods. These results indicate that, in some cases, taxonomically diagnostic characters may be maintained among divergent lineages for millions of years. In other cases, similar phenotypic characters among non-sister taxa, including reproductive strategies, suggest the potential for convergent evolution due to similar selective pressures among distinct lineages. Our analyses provide evidence of population expansions predating the last glacial maximum in the sampled lineages. These results suggest that Pleistocene glaciations were not inherently unfavorable or restrictive for some Melanohalea species, albeit with apparently different demographic histories between sexually and vegetatively reproducing lineages. CONCLUSIONS: Our results contribute to the understanding of how major changes during the Miocene and Pliocene have been important in promoting diversification within common lichen-forming fungi in the northern Hemisphere. Additionally, we provide evidence that glacial oscillations have influenced current population structure of broadly distributed lichenized fungal species throughout the Holarctic.BMC Evolutionary Biology 09/2012; 12(1):176. · 3.52 Impact Factor
Article: A time-calibrated molecular phylogeny of the precious corals: reconciling discrepancies in the taxonomic classification and insights into their evolutionary history.[show abstract] [hide abstract]
ABSTRACT: BACKGROUND: Seamount-associated faunas are often considered highly endemic but isolation and diversification processes leading to such endemism have been poorly documented at those depths. Likewise, species delimitation and phylogenetic studies in deep-sea organisms remain scarce, due to the difficulty in obtaining samples, and sometimes controversial. The phylogenetic relationships within the precious coral family Coralliidae remain largely unexplored and the monophyly of its two constituent genera, Corallium Cuvier and Paracorallium Bayer & Cairns, has not been resolved. As traditionally recognized, the diversity of colonial forms among the various species correlates with the diversity in shape of their supporting axis, but the phylogenetic significance of these characters remains to be tested. We thus used mitochondrial sequence data to evaluate the monophyly of Corallium and Paracorallium and the species boundaries for nearly all named taxa in the family. Species from across the coralliid range, including material from Antarctica, Hawaii, Japan, New Zealand, Taiwan, Tasmania, the eastern Pacific and the western Atlantic were examined. RESULTS: The concatenated analysis of five mitochondrial regions (COI, 16S rRNA, ND2, and ND3-ND6) recovered two major coralliid clades. One clade is composed of two subgroups, the first including Corallium rubrum, the type species of the genus, together with a small group of Paracorallium species (P. japonicum and P. tortuosum) and C. medea (clade I-A); the other subgroup includes a poorly-resolved assemblage of six Corallium species (C. abyssale, C. ducale, C. imperiale, C. laauense, C. niobe, and C. sulcatum; clade I-B). The second major clade is well resolved and includes species of Corallium and Paracorallium (C. elatius, C. kishinouyei, C. konojoi, C. niveum, C. secundum, Corallium sp., Paracorallium nix, Paracorallium thrinax and Paracorallium spp.). A traditional taxonomic study of this clade delineated 11 morphospecies that were congruent with the general mixed Yule-coalescent (GMYC) model. A multilocus species-tree approach also identified the same two well-supported clades, being Clade I-B more recent in the species tree (18.0-15.9 mya) than in the gene tree (35.2-15.9 mya). In contrast, the diversification times for clade-II were more ancient in the species tree (136.4-41.7 mya) than in the gene tree (66.3-16.9 mya). CONCLUSIONS: Our results provide no support for the taxonomic status of the two currently recognized genera in the family Coralliidae. Given that Paracorallium species were all nested within Corallium, we recognize the coralliid genus, Corallium, which includes the type species of the family, and thus consider Paracorallium a junior synonym of Corallium. We propose the use of the genus Hemicorallium Gray for clade I-B (species with long rod sclerites, cylindrical autozooids and smooth axis). Species delimitation in clade I-B remains unclear and the molecular resolution for Coralliidae species is inconsistent in the two main clades. Some species have wide distributions, recent diversification times and low mtDNA divergence whereas other species exhibit narrower allopatric distributions, older diversification times and greater levels of mtDNA resolution.BMC Evolutionary Biology 12/2012; 12(1):246. · 3.52 Impact Factor
Article: Conquering the Sahara and Arabian deserts: Systematics and biogeography of Stenodactylus geckos (Reptilia: Gekkonidae).[show abstract] [hide abstract]
ABSTRACT: BACKGROUND: The evolutionary history of the biota of North Africa and Arabia is inextricably tied to the complex geological and climatic evolution that gave rise to the prevalent deserts of these areas. Reptiles constitute an exemplary group in the study of the arid environments with numerous well-adapted members, while recent studies using reptiles as models have unveiled interesting biogeographical and diversification patterns. In this study, we include 207 specimens belonging to all 12 recognized species of the genus Stenodactylus. Molecular phylogenies inferred using two mitochondrial (12S rRNA and 16S rRNA) and two nuclear (c-mos and RAG-2) markers are employed to obtain a robust time-calibrated phylogeny, as the base to investigate the inter- and intraspecific relationships and to elucidate the biogeographical history of Stenodactylus, a genus with a large distribution range including the arid and hyper-arid areas of North Africa and Arabia. RESULTS: The phylogenetic analyses of molecular data reveal the existence of three major clades within the genus Stenodactylus, which is supported by previous studies based on morphology. Estimated divergence times between clades and sub-clades are shown to correlate with major geological events of the region, the most important of which is the opening of the Red Sea, while climatic instability in the Miocene is hypothesized to have triggered diversification. High genetic variability is observed in some species, suggesting the existence of some undescribed species. The S. petrii - S. stenurus species complex is in need of a thorough taxonomic revision. New data is presented on the distribution of the sister species S. sthenodactylus and S. mauritanicus. CONCLUSIONS: The phylogenetic hypothesis for the genus Stenodactylus presented in this work permits the reconstruction of the biogeographical history of these common desert dwellers and confirms the importance of the opening of the Red Sea and the climatic oscillations of the Miocene as major factors in the diversification of the biota of North Africa and Arabia. Moreover, this study traces the evolution of this widely distributed and highly specialized group, investigates the patterns of its high intraspecific diversity and elucidates its systematics.BMC Evolutionary Biology 12/2012; 12(1):258. · 3.52 Impact Factor