In Press
Worsaae, K., G. Giribet, and A. Martínez. In Press. “The role of progenesis in the diversification of the interstitial annelid lineage Psammodrilidae.” Invertebrate Systematics.
Kallal, R. J., R. Fernández, G. Giribet, and G. Hormiga. In Press. “. A phylotranscriptomic backbone of the orb-weaving spider family Araneidae (Arachnida, Araneae) supported by multiple methodological approaches. .” Molecular Phylogenetics and Evolution.
Giribet, G., R. Buckman-Young, C. Sampaio Costa, C.M. Baker, L. R. Benavides, M. G. Branstetter, S. R. Daniels, and R. Pinto-da-Rocha. In Press. “The "Peripatos" in Eurogondwana?-Lack of evidence that southeast Asian onychophorans walked through Europe. ”.
Sharma, P. P., C. Baker, J. G. Cosgrove, J. Johnson, J. Oberski, R. Raven, M. Harvey, S. Boyer, and G. Giribet. 2018. “A revised dated phylogeny of scorpions: Phylogenomic support for ancient divergence of the temperate Gondwanan family Bothriuridae. .” Molecular Phylogenetics and Evolution 122: 37-45. Abstract
The scorpion family Bothriuridae occupies a subset of landmasses formerly constituting East and West temperate Gondwana, but its relationship to other scorpion families is in question. Whereas morphological data have strongly supported a sister group relationship of Bothriuridae and the superfamily Scorpionoidea, a recent phylogenomic analysis recovered a basal placement of bothriurids within Iurida, albeit sampling only a single exemplar. Here we reexamined the phylogenetic placement of the family Bothriuridae, sampling six bothriurid exemplars representing both East and West Gondwana, using transcriptomic data. Our results demonstrate that the sister group relationship of Bothriuridae to the clade ("Chactoidea" + Scorpionoidea) is supported by the inclusion of additional bothriurid taxa, and that this placement is insensitive to matrix completeness or partitioning by evolutionary rate. We also estimated divergence times within the order Scorpiones using multiple fossil calibrations, to infer whether the family Bothriuridae is sufficiently old to be characterized as a true Gondwanan lineage. We show that scorpions underwent ancient diversification between the Devonian and early Carboniferous. The age interval of the bothriurids sampled (a derived group that excludes exemplars from South Africa) spans the timing of breakup of temperate Gondwana.
Huang, D., G. Hormiga, F. Xia, C. Cai, Z. Yin, Y. Su, and G. Giribet. 2018. “Origin of spiders and their spinning organs illuminated by mid-Cretaceous amber fossils. .” Nature Ecology & Evolution 2: 623-627.
A recent paper in BMC Biology has resolved the family relationships of sea squirts, one of our closest invertebrate relatives, by using a large phylogenomic data set derived from available genomes and newly generated transcriptomes. The work confirms previous ideas that ascidians (the sea squirts) are not monophyletic, as they include some pelagic jelly-like relatives, and proposes a chronogram for a group that has been difficult to resolve due to their accelerated genome evolution.
Giribet, G. 2018. “Current views on chelicerate phylogeny—A tribute to Peter Weygoldt.” Zoologischer Anzeiger 273,: 7-13.
Gainett, G., P. P. Sharma, G. Giribet, and R. H. Willemart. 2018. “Putative adhesive setae on the walking legs of the Paleotropical harvestman Metibalonius sp. (Arachnida: Opiliones: Podoctidae). .” Journal of Arachnology 46: 62-68. Abstract
We provide a first scanning electron microscopy examination of the Paleotropical harvestman family Podoctidae (Opiliones: Laniatores), focusing on the distitarsus of the legs of Metibalonius sp. Distitarsi I and II are mostly equipped with olfactory sensilla chaetica with wall pores, while those of legs III and IV have gustatory sensilla chaetica with a tip pore, ventral trichomes with ovate tips (non-sensory) and a type of spatulate seta. Spatulate setae are present in adults of both sexes, with no apparent sexual dimorphism, but they are absent in the nymph. Seven of these setae are inserted on the frontal surface of the last tarsomere of legs III and IV, with the tips oriented ventrally. Each seta has an s-shaped socketed shaft, which terminates distally in a spatula-shaped structure. The distribution of spatulate setae, restricted to legs III and IV (walking legs), the position on the distitarsi, and the typical spatulate shape suggest an adhesive function for these structures. Morphology and position suggest that the socketed spatulate setae of Metibalonius sp. and the previously reported scopular spatulate setae of other harvestmen constitute two distinct types of adhesive structures, highlighting the diversity of adhesive structures in Laniatores. Future investigations about the natural history of this species and internal morphology of spatulate setae are necessary to test further functional hypotheses and to determine their behavioral role.
Fernández, R., R. J. Kallal, D. Dimitrov, J. A. Ballesteros, M. A. Arnedo, G. Giribet, and G. Hormiga. 2018. “Phylogenomics, diversification dynamics and comparative transcriptomics across the Spider Tree of Life. .” Current Biology.
The interrelationships of the four classes of Myriapoda have been an unresolved question in arthropod phylogenetics and an example of conflict between morphology and molecules. Morphology and development provide compelling support for Diplopoda (millipedes) and Pauropoda being closest relatives, and moderate support for Symphyla being more closely related to the diplopod-pauropod group than any of them are to Chilopoda (centipedes). In contrast, several molecular datasets have contradicted the Diplopoda–Pauropoda grouping (named Dignatha), often recovering a Symphyla–Pauropoda group (named Edafopoda). Here we present the first transcriptomic data including a pauropod and both families of symphylans, allowing myriapod interrelationships to be inferred from phylogenomic data from representatives of all main lineages. Phylogenomic analyses consistently recovered Dignatha with strong support. Taxon removal experiments identified outgroup choice as a critical factor affecting myriapod interrelationships. Diversification of millipedes in the Ordovician and centipedes in the Silurian closely approximates fossil evidence whereas the deeper nodes of the myriapod tree date to various depths in the Cambrian-Early Ordovician, roughly coinciding with recent estimates of terrestrialisation in other arthropod lineages, including hexapods and arachnids.
Voolstra, C., M. Adamski, S. Agrawal, A. Antunes, M. Aranda, Baxevanis, A., M. Blaxter, T. Bosch, H. Bracken-Grissom, and J. Coddington. 2017. “Advancing genomics through the Global Invertebrate Genomics Alliance (GIGA.” Invertebrate Systematics 31: 1-7. Abstract
The Global Invertebrate Genomics Alliance (GIGA), a collaborative network of diverse scientists, marked its second anniversary with a workshop in Munich, Germany in 2015, where international attendees focused on discussing current progress, milestones and bioinformatics resources. The community determined the recruitment and training of talented researchers as one of the most pressing future needs and identified opportunities for network funding. GIGA also promotes future research efforts to prioritise taxonomic diversity and create new synergies. Here, we announce the generation of a central and simple data repository portal with a wide coverage of available sequence data, via the compagen platform, in parallel with more focused and specialised organism databases to globally advance invertebrate genomics. This article serves the objectives of GIGA by disseminating current progress and future prospects in the science of invertebrate genomics with the aim of promotion and facilitation of interdisciplinary and international research.
Schwentner, M., D.J. Combosch, J. P. Nelson, and G. Giribet. 2017. “A phylogenomic solution to the origin of insects by resolving crustacean-hexapod relationships.” Current Biology 27: 1818-1824. Abstract
Insects, the most diverse group of organisms, are nested within crustaceans, arguably the most abundant group of marine animals. However, to date, no consensus has been reached as to which crustacean taxon is the closest relative of hexapods. A majority of studies have proposed that Branchiopoda (e.g., fairy shrimps) is the sister group of Hexapoda [1-7]. However, these investigations largely excluded two equally important taxa, Remipedia and Cephalocarida. Other studies suggested Remipedia [8-11] or Remipedia + Cephalocarida [12, 13] as potential sister groups of hexapods, but they either did not include Cephalocarida or used only Sanger sequence data and morphology [9, 12]. Here we present the first phylogenomic study specifically addressing the origins of hexapods, including transcriptomes for two species each of Cephalocarida and Remipedia. Phylogenetic analyses of selected matrices, ranging from 81 to 1,675 orthogroups and up to 510,982 amino acid positions, clearly reject a sister-group relationship between Hexapoda and Branchiopoda [1-7]. Nonetheless, support for a hexapod sister-group relationship to Remipedia or to Cephalocarida-Remipedia was highly dependent on the employed analytical methodology. Further analyses assessing the effects of gene evolutionary rate and targeted taxon exclusion support Remipedia as the sole sister taxon of Hexapoda and suggest that the prior grouping of Remipedia + Cephalocarida is an artifact, possibly due to long branch attraction and compositional heterogeneity. We further conclude that terrestrialization of Hexapoda probably occurred in the late Cambrian to early Ordovician, an estimate that is independent of their proposed sister group [4, 8, 12, 14].
Bdelloura candida (Platyhelminthes, Tricladida, Maricola) is an ectocommensal symbiont on the American horseshoe crab Limulus polyphemus, living on the book gills and appendages, where it spends its entire life. Given its limited dispersal capabilities and its inability to live outside of the host, we hypothesized a genetic structure that parallels that of its host. We obtained 84 planarian individuals from 19 horseshoe crabs collected from 10 sites from Massachusetts to Florida. We amplified the mitochondrial 16S rRNA and the nuclear internal transcribed spacer 2 and conducted phylogeographic and population genetic analyses, which show a clear and strong genetic break between the populations in the Atlantic and the Gulf coasts. Among the Atlantic populations, two additional, weaker barriers located along Cape Hatteras and Cape Cod restrict gene flow. Even though previous studies have suggested that the populations of the host may be in decline, those of B. candida remain stable, and some even shows signatures of expansion. Our results indicate that the phylogeography of these marine ectocommensal triclads closely mirrors that of its Limulus host, and highlight the challenges to both host and symbiont to genetically connect populations across their distribution.
The existence of the platyhelminth clade Adiaphanida—an assemblage comprising the well‐studied order Tricladida as well as two lesser known taxa, Prolecithophora and the obligate parasitic Fecampiida—is among the more surprising results of flatworm molecular systematics. Each of these three clades is itself largely well‐defined from a morphological point of view, although Adiaphanida at large, despite its strong support in molecular phylogenetic analyses, lacks known morphological synapomorphies. However, one taxon, the genus Genostoma, a parasite of the leptostracan crustacean Nebalia, rests uneasily within its current classification within the fecampiid family Genostomatidae; ultrastructural investigations on this taxon have uncovered a spermatogenesis reminiscent of Kalyptorhynchia, and a dorsal syncytium resembling the neodermatan tegument. Here, we provide molecular sequence data (nearly complete 18S and 28S rRNA) from a representative of Genostoma, with which we test hypotheses on the phylogenetic position of this taxon within Platyhelminthes, expanding upon a recently published phylum‐wide analysis, and applying novel alignment algorithms and substitution models. These analyses unequivocally position Genostoma as the sister group of Prolecithophora. However, even in taxon‐rich analyses, support for the position of the root of Adiaphanida is lacking, highlighting the need for new data types to study the phylogeny of this clade. Interestingly, our analyses also do not recover the monophyly of several taxa previously proposed, notably Continenticola within Tricladida and Protomonotresidae within Prolecithophora. In light of this phylogeny and the distinctive morphology (especially, spermatogenesis) of Genostoma, we advocate for a redefinition of the family Genostomatidae, outside of both Fecampiida and Prolecithophora, to encompass the members of this unique genus of parasites. Within Fecampiida, the family Piscinquilinidae fam. nov. is erected to accommodate the vertebrate‐parasitic Piscinquilinus, formerly Genostomatidae.
Healy, J. M., P. M. Mikkelsen, G. Giribet, and R. Bieler. 2017. “Sperm ultrastructure of the Protobranchia: comparison with other bivalve mollusks and potential taxonomic and phylogenetic significance. .” Fieldiana Zoology 11: 1-28. Abstract
Sperm ultrastructure of nine species of protobranch bivalves, representing three of four extant orders (Solemyida, Nuculida, Nuculanida), is discussed. Greatest diversity occurs in Solemyida (acrosomal vesicle low-conical, tall-conical, or very elongate, with radial plates; nucleus rod-shaped, teardrop-shaped, or very elongate; four, five, or six mitochondria) and the least in Nuculida (acrosomal vesicle low- to tall-conical; lacking radial plates; nucleus rod-shaped, five or six mitochondria) followed by Nuculanida (short, conical acrosomal vesicle with radial plates; spheroidal nucleus; four or five mitochondria). The wide variety of shapes in Solemyidae suggests taxonomic potential, especially in resolution and/or recognition of supraspecific taxa, but no diagnostic family characters were identified. Taxonomic potential exists for Nuculida (acrosomal shape) and Nuculanida (mitochondrial number). Protobranch sperm is highly diverse, and no defining character of the whole group was found. Support was found for the Nuculida and Nuculanida as natural groups but not for their close relationship. Nuculanida and Solemyida exhibit radial plates in the acrosomal vesicle but otherwise share no derived characters. The striking similarity of most sperm features of Nuculanida with certain pteriomorphians, especially Pectinoidea, a relationship also suggested by some mitochondrial DNA sequence data, poses interesting questions concerning their relationships and/or shared functional constraints.
Harvey, M. S., M. G. Rix, D. Harms, G. Giribet, C. J. Vink, and D. E. Walter. 2017. “ The biogeography of Australasian arachnids. .” Ebach, M. C. (Ed.) Handbook of Australasian Biogeography. CRC/Taylor and Francis Group, 241-267.
Giribet, G., and Gregory D. Edgecombe. 2017. “Current understanding of Ecdysozoa and its internal phylogenetic relationships. .” Integrative and Comparative Biology 57: 455-466.
Sironidae, the first described family of Cyphophthalmi, is among the least understood phylogenetically. After examining recent collections across their distribution range, we provide the first comprehensive treatment of Sironidae by including molecular data from most of the known species, and all genera except for the monotypic Odontosiro Juberthie, 1961. We also revisit the male genitalic morphology for most genera by using confocal laser scanning microscopy and provide descriptions of five new species belonging to Iberosiro de Bivort & Giribet, 2004 (monotypic until now), Paramiopsalis Juberthie, 1962 and Siro Latreille, 1802. While the monophyly of Sironidae remains poorly supported using traditional Sanger-based markers, with the Mediterranean Parasiro Hansen & Sørensen, 1904 and the Japanese Suzukielus Juberthie, 1970b sometimes branching basally with respect to the other sironids, the remaining genera form a well-supported Laurentian/Laurasian clade. This group divides into a Western European/North American clade of Siro and the remaining genera, Iberosiro, Paramiopsalis and Cyphophthalmus Joseph, 1868. Iberosiro and Paramiopsalis form a well-supported clade from the NW corner of the Iberian Peninsula, while Cyphophthalmus is widespread in the Balkan region and Eastern Mediterranean. Finally, the following new taxa are described: Iberosiro rosae Giribet, Merino-Sáinz & Benavides, sp. nov., Paramiopsalis anadonae Giribet, Merino-Sáinz & Benavides, sp. nov., Paramiopsalis ramblae Benavides & Giribet, sp. nov., Siro ligiae Giribet, sp. nov., and Siro richarti Benavides & Giribet, sp. nov.
Gilbert, P.U.P.A., K. D. Bergmann, C. E. Myers, M. A. Marcus, R. T. DeVol, C.-Y. Sun, A. Z. Blonsky, J. Zhao, E. A. Karan, and E. Tamre. 2017. “ Nacre tablet thickness records formation temperature in modern and fossil shells. .” Earth and Planetary Science Letters 460: 281-292. Abstract
© 2016 Elsevier B.V. Nacre, the iridescent outer lining of pearls and inner lining of many mollusk shells, is composed of periodic, parallel, organic sheets alternating with aragonite (CaCO 3 ) tablet layers. Nacre tablet thickness (TT) generates both nacre's iridescence and its remarkable resistance to fracture. Despite extensive studies on how nacre forms, the mechanisms controlling TT remain unknown, even though they determine the most conspicuous of nacre's characteristics, visible even to the naked eye. Thermodynamics predicts that temperature (T) will affect both physical and chemical components of biomineralized skeletons. The chemical composition of biominerals is well-established to record environmental parameters, and has therefore been extensively used in paleoclimate studies. The physical structure, however, has been hypothesized but never directly demonstrated to depend on the environment. Here we observe that the physical TT in nacre from modern and fossil shallow-water shells of the bivalves Pinna and Atrina correlates with T as measured by the carbonate clumped isotope thermometer. Based on the observed TT vs. T correlation, we anticipate that TT will be used as a paleothermometer, useful to estimate paleotemperature in shallow-water paleoenvironments. Here we successfully test the proposed new nacre TT thermometer on two Jurassic Pinna shells. The increase of TT with T is consistent with greater aragonite growth rate at higher T, and with greater metabolic rate at higher T. Thus, it reveals a complex, T-dependent biophysical mechanism for nacre formation.
Gainett, G., P. Michalik, C. H. G. Müller, G. Giribet, G Talarico, and R. H. Willemart. 2017. “Putative thermo-/hygroreceptive tarsal sensilla on the sensory legs of an armored harvestman (Arachnida, Opiliones).” Zoologischer Anzeiger 270: 81-97. Abstract
Most harvestman species are dependent on high humidity levels and amenable temperatures for homeostasis. While they are known to actively choose environments with these conditions, no thermo-/hygroreceptor has yet been identified in harvestmen. Using electron microscopy, we investigated the ultrastructure of two types of hair sensilla of the armored harvestman Heteromitobates discolor (Laniatores, Gonyleptidae): namely the sensillum basiconicum and the hooded sensillum. Both structures occur in small numbers (sensilla basiconica: 28 units; hooded sensilla: 4 units) and are distributed on the distal parts of the legs. On the distalmost tarsomeres I and II, the receptor cells of paired sensilla basiconica and single hooded sensillum form a common axon bundle proceeding towards the tarsal nerve. The sensillum basiconicum is innervated by 3-4 dendrites and has a longitudinal slit giving the impression of a shaft with two flaps, resembling a beak. The slit probably allows for evaporation of sensillum lymph. The hooded sensillum is innervated by two bundles of three dendrites each, has two pore-like structures on its tip and displays an unusual reticulate cuticle of the shaft. Details of shaft cuticle, the evidence of evaporation of sensillum lymph, and specific innervation patterns support our hypothesis that sensilla basiconica are thermo- and/or hygroreceptors. Even though the definite function of hooded sensilla remains unclear, its putative receptor modalities are assessed by means of specific ultrastructures. Moreover, we discuss with regard to functional ultrastructures as to whether the evaporation system of sensilla basiconica fits mechanisms of hygroreception as known from current literature. Finally, we discuss potentials and purpose given by spatial coherence of both types of sensilla at the tip of the sensory appendages.
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