Publications

In Press
Fernandez, R., G.D. Edgecombe, and G. Giribet. In Press. “Exploring phylogenomic relationships within Myriapoda: should high matrix occupancy be the goal?.” bioRxiv. Publisher's VersionAbstract

Myriapods are one of the dominant terrestrial arthropod groups including the diverse and familiar centipedes and millipedes. Although molecular evidence has shown that Myriapoda is monophyletic, its internal phylogeny remains contentious and understudied, especially when compared to those of Chelicerata and Hexapoda. Until now, efforts have focused on taxon sampling (e.g., by including a handful of genes in many species) or on maximizing matrix occupancy (e.g., by including hundreds or thousands of genes in just a few species), but a phylogeny maximizing sampling at both levels remains elusive. In this study, we analyzed forty Illumina transcriptomes representing three myriapod classes (Diplopoda, Chilopoda and Symphyla); twenty-five transcriptomes were newly sequenced to maximize representation at the ordinal level in Diplopoda and at the family level in Chilopoda. Eight supermatrices were constructed to explore the effect of several potential phylogenetic biases (e.g., rate of evolution, heterotachy) at three levels of mean gene occupancy per taxon (50%, 75% and 90%). Analyses based on maximum likelihood and Bayesian mixture models retrieved monophyly of each myriapod class, and resulted in two alternative phylogenetic positions for Symphyla, as sister group to Diplopoda + Chilopoda, or closer to Diplopoda, the latter hypothesis having been traditionally supported by morphology. Within centipedes, all orders were well supported, but two nodes remained in conflict in the different analyses despite dense taxon sampling at the family level, situating the order Scolopendromorpha as sister group to a morphologically-anomalous grouping of Lithobiomorpha + Geophilomorpha in a subset of analyses. Interestingly, this anomalous result was obtained for all analyses conducted with the most complete matrix (90% of occupancy), being at odds not only with the sparser but more gene-rich supermatrices (75% and 50% supermatrices) or with the matrices optimizing phylogenegic informativeness and the most conserved genes, but also with previous hypotheses based on morphology, development or other molecular data sets. We discuss the implications of these findings in the context of the ever more prevalent quest for completeness in phylogenomic studies.

Giribet, G., and G. Y. Kawauchi. In Press. “How many species of Siphonaria pectinata (Gastropoda: Heterobranchia) are there?.” Journal of Molluscan Studies, doi: 10.1093/mollus/eyv038. Publisher's VersionAbstract

Siphonaria pectinata (Linnaeus, 1758) has been considered a widespread species with Amphiatlantic distribution or a case of cryptic taxonomy where sibling species exist. We undertook molecular evaluation of 66 specimens from across its putative distribution range. We examined up to three molecular markers (mitochondrial cytochrome c oxidase subunit I and 16S rRNA, and nuclear internal transcribed spacer-2) of putative S. pectinata, including populations from the Mediterranean Sea, eastern Atlantic (Spain, Canary Islands, Cape Verde Islands, Cameroon and Gabon) and western Atlantic (Florida and Mexico), covering most of the natural range of the species. While little information could be derived from the shell morphology, molecular data clearly distinguished three lineages with no apparent connectivity. These lineages correspond to what we interpret as three species, two suspected from prior work: S. pectinata, restricted to the eastern Atlantic and Mediterranean and S. naufragum Stearns, 1872 in Florida and the Gulf of Mexico. A third species has been identified for the Cape Verde Archipelago, for which we use the available name S. placentula Menke, 1853.

Giribet, G. In Press. “New Animal Phylogeny: Future challenges for animal phylogeny in the age of phylogenomics.” Organisms Diversity & Evoution, 1-8. Berlin Heidelberg: Springer, 1-8. Publisher's VersionAbstract

The science of phylogenetics, and specially the subfield of molecular systematics, has grown exponentially not only in the amount of publications and general interest, but also especially in the amount of genetic data available. Modern phylogenomic analyses use large genomic and transcriptomic resources, yet a comprehensive molecular phylogeny of animals, including the newest types of data for all phyla, remains elusive. Future challenges need to address important issues with taxon sampling—especially for rare and small animals—orthology assignment, algorithmic developments, and data storage and to figure out better ways to integrate information from genomes and morphology in order to place fossils more precisely in the animal tree of life. Such precise placement will also aid in providing more accurate dates to major evolutionary events during the evolution of our closest kingdom.

Clouse, R.M., P. P. Sharma, J.C. Stuart, L.R. Davis, G. Giribet, S.L. Boyer, and W.C. Wheeler. In Press. “Phylogeography of the harvestman Metasiro (Arthropoda, Arachnida, Opiliones) reveals a potential solution to the Pangean paradox..” Organisms Diversity & Evoution, 1-18. Berlin Heidelberg: Springer, 1-18. Publisher's VersionAbstract

At both global and local scales, mite harvestmen (Opiliones, Cyphophthalmi) have been shown to have achieved their current global distribution strictly through vicariance. However, the implicit low dispersal capability of this group does not explain how they expand their ranges and come to occupy enormous landmasses prior to rifting. To investigate at the population level the limited vagility that characterizes the suborder generally, and how its dispersal capacity determines diversification dynamics, range expansion, and historical biogeography, we examined as a test case the phylogeography of the genus Metasiro. This genus consists of three widely separated, morphologically cryptic species that inhabit the Southeastern United States. Distances between sampling sites spanned a range of geographic scales, from 4 m to over 500 km. Population structure was inferred from fragments of six loci (three mitochondrial, three nuclear) amplified from 221 specimens. We tested for population structure and gene flow, constructed a dated phylogeny of the genus, and developed a program for estimating the effective population size with confidence intervals. Individuals of Metasiro americanus demonstrate remarkable population structure at scales of less than 25 m, but populations vary in their haplotypic diversity, and some exhibit evidence of historical gene flow. The estimated timing of cladogenesis within the genus accords closely with the geological history of the North American coastline, and the three species are at the endpoints of large watersheds. This suggests that mite harvestman lineages expand their ranges by hydrochory, providing for the first time a plausible mechanism whereby these animals dispersed across Pangea despite their low vagility in stable environments.

2015
Riesgo, A., M. Maldonado, S. Lopez-Legentil, and G. Giribet. 2015. “A Proposal for the Evolution of Cathepsin and Silicatein in Sponges.” J Mol Evol 80: 278-91.Abstract

Cathepsins are enzymes capable of degrading proteins intracellularly. They occur ubiquitously in opisthokonts, but their potential to provide insight across the evolutionary transition from protists to metazoans remains poorly investigated. Here, we explore the evolution of cathepsins using comparative analyses of transcriptomic datasets, focusing on both, protists (closely related to metazoans), and early divergent animals (i.e., sponges). We retrieved DNA sequences of nine cathepsin types (B, C, D, F, H, L, O, Z, and silicatein) in the surveyed taxa. In choanoflagellates, only five types (B, C, L, O, Z) were identified, all of them being also found in sponges, indicating that while all cathepsins present in protists were conserved across metazoan lineages, cathepsins F and H (and probably D) are metazoan acquisitions. The phylogeny of cysteine protease cathepsins (excluding cathepsin D) revealed two major lineages: lineage B (cathepsins B and C) and lineage L (cathepsins F, H, L, O, Z). In the latter lineage, a mutation at the active site of cathepsin L gave rise to silicatein, an enzyme exclusively known to date from siliceous sponges and involved in the production of their silica spicules. However, we found that several sponges with siliceous spicules did not express silicatein genes and that, in contrast, several aspiculate sponges did contain silicatein genes. Our results suggest that the ability to silicify may have evolved independently within sponges, some of them losing this capacity secondarily. We also show that most phylogenies based on cathepsin and silicatein genes (except for that of cathepsin O) failed to recover the major lineages of sponges.

Giribet, G., and P. P. Sharma. 2015. “Evolutionary biology of harvestmen (arachnida, opiliones).” Annu Rev Entomol 60: 157-75.Abstract

Opiliones are one of the largest arachnid orders, with more than 6,500 species in 50 families. Many of these families have been erected or reorganized in the last few years since the publication of The Biology of Opiliones. Recent years have also seen an explosion in phylogenetic work on Opiliones, as well as in studies using Opiliones as test cases to address biogeographic and evolutionary questions more broadly. Accelerated activity in the study of Opiliones evolution has been facilitated by the discovery of several key fossils, including the oldest known Opiliones fossil, which represents a new, extinct suborder. Study of the group's biology has also benefited from rapid accrual of genomic resources, particularly with respect to transcriptomes and functional genetic tools. The rapid emergence and utility of Phalangium opilio as a model for evolutionary developmental biology of arthropods serve as demonstrative evidence of a new area of study in Opiliones biology, made possible through transcriptomic data.

Gonzalez, V. L., S. C. Andrade, R. Bieler, T. M. Collins, C. W. Dunn, P. M. Mikkelsen, J. D. Taylor, and G. Giribet. 2015. “A phylogenetic backbone for Bivalvia: an RNA-seq approach.” Proc Biol Sci 282: 20142332.Abstract

Bivalves are an ancient and ubiquitous group of aquatic invertebrates with an estimated 10 000-20 000 living species. They are economically significant as a human food source, and ecologically important given their biomass and effects on communities. Their phylogenetic relationships have been studied for decades, and their unparalleled fossil record extends from the Cambrian to the Recent. Nevertheless, a robustly supported phylogeny of the deepest nodes, needed to fully exploit the bivalves as a model for testing macroevolutionary theories, is lacking. Here, we present the first phylogenomic approach for this important group of molluscs, including novel transcriptomic data for 31 bivalves obtained through an RNA-seq approach, and analyse these data with published genomes and transcriptomes of other bivalves plus outgroups. Our results provide a well-resolved, robust phylogenetic backbone for Bivalvia with all major lineages delineated, addressing long-standing questions about the monophyly of Protobranchia and Heterodonta, and resolving the position of particular groups such as Palaeoheterodonta, Archiheterodonta and Anomalodesmata. This now fully resolved backbone demonstrates that genomic approaches using hundreds of genes are feasible for resolving phylogenetic questions in bivalves and other animals.

Lemer, S., G. Y. Kawauchi, S. C. Andrade, V. L. Gonzalez, M. J. Boyle, and G. Giribet. 2015. “Re-evaluating the phylogeny of Sipuncula through transcriptomics.” Mol Phylogenet Evol 83: 174-83.Abstract

Sipunculans (also known as peanut worms) are an ancient group of exclusively marine worms with a global distribution and a fossil record that dates back to the Early Cambrian. The systematics of sipunculans, now considered a distinct subclade of Annelida, has been studied for decades using morphological and molecular characters, and has reached the limits of Sanger-based approaches. Here, we reevaluate their family-level phylogeny by comparative transcriptomic analysis of eight species representing all known families within Sipuncula. Two data matrices with alternative gene occupancy levels (large matrix with 675 genes and 62% missing data; reduced matrix with 141 genes and 23% missing data) were analysed using concatenation and gene-tree methods, yielding congruent results and resolving each internal node with maximum support. We thus corroborate prior phylogenetic work based on molecular data, resolve outstanding issues with respect to the familial relationships of Aspidosiphonidae, Antillesomatidae and Phascolosomatidae, and highlight the next area of focus for sipunculan systematics.

Andrade, SCS., M. Novo, G. Y. Kawauchi, K. Worsaae, F Pleijei, G. Giribet, and G. W. Rouse. 2015. “Articulating "archiannelids": Phylogenomics and annelid relationships, with emphasis on meiofaunal taxa..” Molecular Biology and Evolution 32: 2860-2875.
Fernandez, R., S. Lemer, E. McIntyre, and G. Giribet. 2015. “Comparative phylogeography and population genetic structure of three widespread mollusc species in the Mediterranean and near Atlantic.” Marine Ecology 36: 96-103.
Dreszer, TB., T. Radja, and G. Giribet. 2015. “Cyphophthalmus solentiensis sp. nov. (Cyphophthalmi, Sironidae) a new endogean mite harvestman species from Croatia, with an application of confocal laser microscopy to illustrate genitalia in Opiliones..” Breviora 543: 1-15.
Giribet, G. 2015. “Morphology should not be forgotten in the era of genomics-a phylogenetic perspective.” Zoologischer Anzeriger 256: 96-103.
Kvist, S., AV. Chernyshev, and G. Giribet. 2015. “Phylogeny of Nemertea with special interest in the placement of diversity from Far East Russia and northeast Asia..” Hydrobiologia 760: 105-119.
Groh, S, and G. Giribet. 2015. “Polyphyly of Caddoidea, reinstatement of the family Acropsopilionidae in Dyspnoi, and a revised classification system of Palpatores (Arachnida, Opiliones).” Cladistics 31: 277-290.
Herrera-Bachiller, A, S. Kvist, G. Giribet, and J. Junoy. 2015. “Redescription of Micrura dellechiajei (Hubrecht, 1879) (Nemertea, Pilidiophora, Lineidae), a rare Mediterranean species..” Journal of the Marine Biological Association of the U.K. 95: 1091-1100.
Edgecombe, GD., V. Vahtera, G. Giribet, and P. Kaunisto. 2015. “Species limits and phylogeography of Newportia (Scolopendromorpha) and implications for widespread morphospecies..” ZooKeys 510: 65-77.
Laumer, CE, N. Bekkouche, Kerbl A, F. Goetz, RC. Neves, MV. Sorensen, RM. Kristensen, A. Hejnol, CW. Dunn, and G. Giribet. 2015. “Spiralian phylogeny informs the evolution of microscopic lineages.” Current Biology 25: 2000-2006.
Novo, M, R. Fernandez, D. Fernandez Marchan, D. Trigo, DJ. Diaz Cosin, and G. Giribet. 2015. “Unearthing the historical biogeography of Mediterranean earthworms (Annelida: Hormogastridae).” Journal of Biogeogrpahy 42: 751-762.
Fernandez, R, and G. Giribet. 2015. “Unnoticed in the tropics: phylogenomic resolution of the poorly known arachnid order Ricinulei (Arachnida).” Royal Society Open Science 2: 150065.
Laumer, C. E., A. Hejnol, and G. Giribet. 2015. “Nuclear genomic signals of the 'microturbellarian' roots of platyhelminth evolutionary innovation.” Elife 4.Abstract

Flatworms number among the most diverse invertebrate phyla and represent the most biomedically significant branch of the major bilaterian clade Spiralia, but to date, deep evolutionary relationships within this group have been studied using only a single locus (the rRNA operon), leaving the origins of many key clades unclear. In this study, using a survey of genomes and transcriptomes representing all free-living flatworm orders, we provide resolution of platyhelminth interrelationships based on hundreds of nuclear protein-coding genes, exploring phylogenetic signal through concatenation as well as recently developed consensus approaches. These analyses robustly support a modern hypothesis of flatworm phylogeny, one which emphasizes the primacy of the often-overlooked 'microturbellarian' groups in understanding the major evolutionary transitions within Platyhelminthes: perhaps most notably, we propose a novel scenario for the interrelationships between free-living and vertebrate-parasitic flatworms, providing new opportunities to shed light on the origins and biological consequences of parasitism in these iconic invertebrates.

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