ALBERT

Description: Gene regulatory networks (GRN) are central to developmental processes. They are composed of transcription factors and signaling molecules orchestrating gene expression modules that tightly regulate the development of organisms. The neural crest (NC) is a multipotent cell population that is considered a key innovation of vertebrates. Its derivatives contribute to shaping the astounding morphological diversity of jaws, teeth, head skeleton, or pigmentation. Here, we study the molecular evolution of the NC GRN by analyzing patterns of molecular divergence for a total of 36 genes in 16 species of bony fishes. Analyses of nonsynonymous to synonymous substitution rate ratios (d N /d S ) support patterns of variable selective pressures among genes deployed at different stages of NC development, consistent with the developmental hourglass model. Model-based clustering techniques of sequence features support the notion of extreme conservation of NC-genes across the entire network. Our data show that most genes are under strong purifying selection that is maintained throughout ray-finned fish evolution. Late NC development genes reveal a pattern of increased constraints in more recent lineages. Additionally, seven of the NC-genes showed signs of relaxation of purifying selection in the famously species-rich lineage of cichlid fishes. This suggests that NC genes might have played a role in the adaptive radiation of cichlids by granting flexibility in the development of NC-derived traits—suggesting an important role for NC network architecture during the diversification in vertebrates.

Description: Beetles represent the largest insect order and they display extreme morphological, ecological and behavioral diversity, which makes them ideal models for evolutionary studies. Here, we present the draft genome of the scarab beetle Oryctes borbonicus , which has a more basal phylogenetic position than the two previously sequenced pest species Tribolium castaneum and Dendroctonus ponderosae providing the potential for sequence polarization. Oryctes borbonicus is endemic to La Réunion, an island located in the Indian Ocean, and is the host of the nematode Pristionchus pacificus , a well-established model organism for integrative evolutionary biology. At 518 Mb, the O. borbonicus genome is substantially larger and encodes more genes than T. castaneum and D. ponderosae . We found that only 25% of the predicted genes of O. borbonicus are conserved as single copy genes across the nine investigated insect genomes, suggesting substantial gene turnover within insects. Even within beetles, up to 21% of genes are restricted to only one species, whereas most other genes have undergone lineage-specific duplications and losses. We illustrate lineage-specific duplications using detailed phylogenetic analysis of two gene families. This study serves as a reference point for insect/coleopteran genomics, although its original motivation was to find evidence for potential horizontal gene transfer (HGT) between O. borbonicus and P. pacificus . The latter was previously shown to be the recipient of multiple horizontally transferred genes including some genes from insect donors. However, our study failed to provide any clear evidence for additional HGTs between the two species.

Description: Cichlid fishes are an ideal model system for studying biological diversification because they provide textbook examples of rapid speciation. To date, there has been little focus on the role of gene regulation during cichlid speciation. However, in recent years, gene regulation has been recognized as a powerful force linking diversification in gene function to speciation. Here, we investigated the potential role of miRNA regulation in the diversification of six cichlid species of the Midas cichlid lineage ( Amphilophus spp.) inhabiting the Nicaraguan crater lakes. Using several genomic resources, we inferred 236 Midas miRNA genes that were used to predict the miRNA target sites on 8,232 Midas 3'-UTRs. Using population genomic calculations of SNP diversity, we found the miRNA genes to be more conserved than protein coding genes. In contrast to what has been observed in other cichlid fish, but similar to what has been typically found in other groups, we observed genomic signatures of purifying selection on the miRNA targets by comparing these sites with the less conserved nontarget portion of the 3'-UTRs. However, in one species pair that has putatively speciated sympatrically in crater Lake Apoyo, we recovered a different pattern of relaxed purifying selection and high genetic divergence at miRNA targets. Our results suggest that sequence evolution at miRNA binding sites could be a critical genomic mechanism contributing to the rapid phenotypic evolution of Midas cichlids.

Description: Horizontal gene transfer (HGT) has been recognized to be an important mechanism that shaped the evolution and genomes of prokaryotes and unicellular eukaryotes. However, HGT is regarded to be exceedingly rare among eukaryotes. We discovered massive transfers of a DNA transposon, a Tc1 element encoding a transposase, between multiple teleost fishes and lampreys that last shared a common ancestor over 500 Ma. Members of this group of Tc1 elements were found to exhibit a mosaic phylogenetic distribution, yet their sequences were highly similar even between distantly related lineages (95%–99% identity). Our molecular phylogenetic analyses suggested that horizontal transfers of this element happened repeatedly, involving multiple teleost fishes that are phylogenetically only distantly related. Interestingly, almost all the affected teleost lineages are also known to be subject to lamprey parasitism, suggesting that the horizontal transfers between vertebrates might have occurred through parasite–host interaction. The genomes of several northern hemisphere lamprey species, including that of the sea lamprey ( Petromyzon marinus ), were found to contain thousands of copies of the foreign elements. Impact of this event is discussed in relation to other peculiar genomic features of lampreys.

Description: Field evidence from the Baladiyah complex in the northern part of the Arabian–Nubian Shield of Saudi Arabia indicates several erosional unconformities separating different high- and medium-grade metasedimentary sequences. This suggests that the collision between East and West Gondwana involved several cycles of exhumation and burial, providing a unique opportunity to study the multiple stages of this orogeny. A mineral equilibria approach and thermodynamic modeling are used to place constraints on the formation conditions of each of these cycles. It is shown that the complex is characterized by three regional metamorphic events followed by a fourth metamorphic event related to shear heating owing to the thrusting of post-tectonic granites. During the first metamorphic event peak metamorphism was at around 705–715°C and 5·2–5·6 kbar followed by subsequent decompression to the Earth’s surface. Subsequently deposited sediments attained 635–670°C and 4·2–5 kbar during a second metamorphic event, followed by exhumation, erosion and deposition of molasse sediments. The rocks were then buried for a third time and metamorphosed to greenschist-facies metamorphic conditions (330 ± 30°C and 3·6–4·6 kbar) under the load of the molasse sediments. Finally, post-tectonic granites were intruded and thrust during the final Pan-African exhumation, causing a fourth metamorphic event (700 ± 25°C). Correlation of this metamorphic evolution with the deformation history shows that the first and the second metamorphic events occurred in a compressional regime (D 1 and D 2 ), interpreted to be related to the first (750 Ma) and the second (676 Ma) collision stages between East and West Gondwana, respectively. The third deformation phase began with a compressional regime causing the third metamorphic event, and then turned into an oblique transpressive regime, which led to escape tectonics and the development of the large-scale Najd strike-slip shear zone system.

Description: We have recently shown that the human Nuclear pore-associated protein ( NPAP1 ) /C15orf2 gene encodes a nuclear pore-associated protein. This gene is one of several paternally expressed imprinted genes in the genomic region 15q11q13. Because the Prader–Willi syndrome is known to be caused by the loss of function of paternally expressed genes in 15q11q13, a phenotypic contribution of NPAP1 cannot be excluded. NPAP1 appears to be under strong positive Darwinian selection in primates, suggesting an important function in primate biology. Interestingly, however, in contrast to all other protein-coding genes in 15q11q13, NPAP1 has no ortholog in the mouse. Our investigation of the evolutionary origin of NPAP1 showed that the gene is specific to primate species and absent from the 15q11q13-orthologous regions in all nonprimate mammals. However, we identified a group of paralogous genes, which we call NPAP1L , in all placental mammals except rodents. Phylogenetic analysis revealed that NPAP1 , NPAP1L , and another group of genes ( UPF0607 ), which is also restricted to primates, are closely related to the vertebrate transmembrane nucleoporin gene POM121 , although they lack the transmembrane domain. These three newly identified groups of genes all lack conserved introns, and hence, are likely retrogenes. We hypothesize that, in the common ancestor of placentals, the POM121 gene retrotransposed and gave rise to an NPAP1 -ancestral retrogene NPAP1L/NPAP1/UPF0607 . Our results suggest that the nuclear pore-associated gene NPAP1 originates from the vertebrate nucleoporin gene POM121 and—after several steps of retrotransposition and duplication—has been subjected to genomic imprinting and positive selection after integration into the imprinted SNRPN-UBE3A chromosomal domain.

Description: The H.U. Sverdrupfjella is part of the high-grade Maud Belt in Dronning Maud Land (East Antarctica), which was located in a central position of the Gondwana supercontinent. Here we study high-pressure granulites from the eastern H.U. Sverdrupfjella and present a detailed reconstruction of the P–T–t history based on a combination of Zr-in-rutile and Ti-in-zircon thermometry, zircon U–Pb dating, monazite chemical dating, garnet diffusion modelling and petrological modelling. Peak metamorphic conditions of ~930°C and 1·45 GPa persisted for less than 6 Myr and were attained at 570 ± 7 Ma, embedded in a well-documented clockwise loading, heating, and decompression path. The rocks had already been rapidly exhumed to a crustal depth of ~30 km at 556 ± 7 Ma. In addition to the very short-lived ultrahigh-temperature peak, zircon preserves evidence for protracted granulite-facies conditions with temperatures above 800°C from as early as c. 590 Ma, persisting for c. 40 Myr. Constraints on prograde metamorphism are recorded in zircon and in rutile inclusions in garnet. Zr-in-rutile thermometry using rutile included in different generations of garnet is used to reconstruct the prograde P–T path, documenting burial followed by heating to ultrahigh temperatures at peak pressures. Complementary Ti zonation in prograde cores of zircon grains documents and dates heating and peak temperatures, whereas younger zircon rims show lower Ti-in-zircon temperatures and date the retrograde stages of metamorphism. Our results provide the first evidence for Neoproterozoic high-pressure granulite-facies metamorphism and ultrahigh-temperature conditions for this region. The clockwise loading–heating path and the peak P–T conditions strongly indicate that the rocks preserved in Dronning Maud Land were part of the lower plate during a continent–continent collision event related to Gondwana assembly at c. 570 Ma. The metamorphic evolution determined in this study and the correlation with similar P–T evolutions documented in adjacent terranes favour the continuation of the c. 580–560 Ma Mozambique Belt into Dronning Maud Land. Furthermore, the striking contemporaneity of the metamorphism in the different parts of central Gondwana suggests that the Coats Land Block was part of greater India prior to this collision.

Description: LINE- Alu -VNTR- Alu -like (LAVA) elements comprise a family of non-autonomous, composite, non-LTR retrotransposons specific to gibbons and may have played a role in the evolution of this lineage. A full-length LAVA element consists of portions of repeats found in most primate genomes: CT-rich, Alu -like, and VNTR regions from the SVA retrotransposon, and portions of the Alu Sz and L1ME5 elements. To evaluate whether the gibbon genome currently harbors functional LAVA elements capable of mobilization by the endogenous LINE-1 (L1) protein machinery and which LAVA components are important for retrotransposition, we established a trans -mobilization assay in HeLa cells. Specifically, we tested if a full-length member of the older LAVA subfamily C that was isolated from the gibbon genome and named LAVA C , or its components, can be mobilized in the presence of the human L1 protein machinery. We show that L1 proteins mobilize the LAVA C element at frequencies exceeding processed pseudogene formation and human SVA E retrotransposition by 〉 100-fold and ≥3-fold, respectively. We find that only the SVA-derived portions confer activity, and truncation of the 3' L1ME5 portion increases retrotransposition rates by at least 100%. Tagged de novo insertions integrated into intronic regions in cell culture, recapitulating findings in the gibbon genome. Finally, we present alternative models for the rise of the LAVA retrotransposon in the gibbon lineage.

Description: The members of the paired box ( Pax ) family regulate key developmental pathways in many metazoans as tissue-specific transcription factors. Vertebrate genomes typically possess nine Pax genes ( Pax1–9 ), which are derived from four proto- Pax genes in the vertebrate ancestor that were later expanded through the so-called two-round (2R) whole-genome duplication. A recent study proposed that pax6a genes of a subset of teleost fishes (namely, acanthopterygians) are remnants of a paralog generated in the 2R genome duplication, to be renamed pax6.3 , and reported one more group of vertebrate Pax genes ( Pax6.2 ), most closely related to the Pax4/6 class. We propose to designate this new member Pax10 instead and reconstruct the evolutionary history of the Pax4/6/10 class with solid phylogenetic evidence. Our synteny analysis showed that Pax4 , - 6 , and - 10 originated in the 2R genome duplications early in vertebrate evolution. The phylogenetic analyses of relationships between teleost pax6a and other Pax4 , -6 , and -10 genes, however, do not support the proposed hypothesis of an ancient origin of the acanthopterygian pax6a genes in the 2R genome duplication. Instead, we confirmed the traditional scenario that the acanthopterygian pax6a is derived from the more recent teleost-specific genome duplication. Notably, Pax6 is present in all vertebrates surveyed to date, whereas Pax4 and -10 were lost multiple times in independent vertebrate lineages, likely because of their restricted expression patterns: Among Pax6 -positive domains, Pax10 has retained expression in the adult retina alone, which we documented through in situ hybridization and quantitative reverse transcription polymerase chain reaction experiments on zebrafish, Xenopus , and anole lizard.

Description: The ectodermal neural cortex ( ENC ) gene family, whose members are implicated in neurogenesis, is part of the kelch repeat superfamily. To date, ENC genes have been identified only in osteichthyans, although other kelch repeat-containing genes are prevalent throughout bilaterians. The lack of elaborate molecular phylogenetic analysis with exhaustive taxon sampling has obscured the possible link of the establishment of this gene family with vertebrate novelties. In this study, we identified ENC homologs in diverse vertebrates by means of database mining and polymerase chain reaction screens. Our analysis revealed that the ENC3 ortholog was lost in the basal eutherian lineage through single-gene deletion and that the triplication between ENC1 , -2, and -3 occurred early in vertebrate evolution. Including our original data on the catshark and the zebrafish, our comparison revealed high conservation of the pleiotropic expression pattern of ENC1 and shuffling of expression domains between ENC1, -2, and -3 . Compared with many other gene families including developmental key regulators, the ENC gene family is unique in that conventional molecular phylogenetic inference could identify no obvious invertebrate ortholog. This suggests a composite nature of the vertebrate-specific gene repertoire, consisting not only of de novo genes introduced at the vertebrate origin but also of long-standing genes with no apparent invertebrate orthologs. Some of the latter, including the ENC gene family, may be too rapidly evolving to provide sufficient phylogenetic signals marking orthology to their invertebrate counterparts. Such gene families that experienced saltatory evolution likely remain to be explored and might also have contributed to phenotypic evolution of vertebrates.