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Nonetheless, two cases of cross-class viral transmissions were observed. Thus, this particular finding should be interpreted with caution. Nevertheless, since there was only one lobe-finned fish FLERV ie, CoeEFV in their study, robust statistical analyses could not be performed to verify the co-speciation, and limited data could obscure a history of viral cross-species transmissions.

Thus, both the phylogenetic placement and temporal origins of CoeEFV are not consistent with co-speciation nor do they provide evidence for a marine origin of FVs. Instead, the branching date of lobe-finned fish FLERVs falls within the period when therapsids—a group of mammal-like reptiles—diversified and dominated the land Together, our results suggest that lobe-finned fish FV-like viruses do not have a marine origin, but instead originated from one or a series of cross-class transmissions that happened in the middle Permian, ultimately from a prehistoric therapsid to a lobe-finned fish.

Combined with the observed phylogenetic pattern, these date estimates support the hypothesis of a marine origin of FVs. To our knowledge, this is the oldest date ever directly inferred for any viruses, greater than the age estimate of the oldest known dsDNA viruses by Myr Myr old Our results offer key insights into the early history of retroviral evolution as a whole. While retroviruses can be found throughout marine and terrestrial vertebrates, with fish and marine tetrapod ERVs sometimes shown to be basal 1 , 2 , robust temporal and phylogenetic evidence of their ancient origins has been lacking.

The discovery of ancient orthologous ERVs has shed some light on the origin of retroviruses. However, the oldest known orthologous ERVs are only Myr old, providing evidence of their existence during the early diversification of mammals 4. Virus-host co-speciation is another source of information that can be integrated into analyses to infer the age of viruses, but again, the oldest retroviral age estimate that was derived based on virus-host co-speciation pattern is only Myr old 5 , 6.

Furthermore, we also found that fish FLERVs are positioned towards the root of the tree, pointing towards a marine origin of retroviruses. The scope of the screening was limited to vertebrates, excluding mammals taxid: The screening was performed in a stepwise manner. In the first iteration, the number of target contigs was set to When there were more than three RT sequences on one contig, only the best three ranked under the default tBLASTn settings were kept for further analyses.

Together with RT sequences of known alpha-, beta-, gamma-, delta- epsilon-, lenti- and spuma-retroviruses, the phylogenetic relationships of these RT sequences were estimated under the maximum-likelihood ML framework by using RAxML Bootstrap clade support values were calculated using 1, pseudoreplicates. We used this RT tree to broadly classify viral sequences into various established retrovirus genera.

To retrieve more RT sequences, the screening process was then repeated with increasing target contig numbers , , and 1, until no additional species were identified as containing FV-like RT sequences. For the final tree, a Bayesian maximum clade credibility phylogeny was also reconstructed to confirm the result, by using MrBayes 3. A metropolis coupling algorithm 3 hot and 1 cold chains was applied to improve the sampling. The alignment aa, sequences is available from the authors upon request. The RT tree is shown in Fig.

The numbers of the target contigs were set to for the nr, est, HTGS and TSA database screening, and 1, for the wgs database screening. These settings were used as they were sufficient to identify all species containing FV-like RT sequences in the first round of screening, in which the RT sequence of CoeEFV was used as a probe. BLAST hits from additional species were added to the phylogenetic analyses to determine whether or not they are FV-like.

The alignments used for the ancestral sequence inferences are available from the authors upon request. MEGA 6 ref. We then divided the distance between paired LTRs by two to obtain a total per-lineageLTR substitution estimate, which in turn was divided by the rate of the LTR evolution to derive the time it took to accumulate the observed number of substitutions, ie, their age.

We assumed that the LTR rate of evolution is equal to the neutral rate of the host genome. To investigate phylogenetic relationships between FVs and FLERVs in more detail, we estimated their phylogeny based on a manually curated Pol protein alignment aa. In the case of fish FLERVs, they were not used because they could not be aligned to those of mammalian FVs due to high sequence divergence.

As a result, only Pol proteins were used to reconstruct the phylogeny. Class III retroviruses were used to root the tree. The alignment is available from the authors upon request. The phylogeny was estimated under the Bayesian framework by using MrBayes 3. No molecular clock was imposed that is, a non-clock and unconstrained tree. A metropolis coupling algorithm 3 hot and 1 cold chains was applied to improve the MCMC sampling.

To estimate its phylogenetic position, a separate Gag phylogeny of salamander FLERVs was estimated by using the same method. The alignment of Gag aa is also available from the authors upon request. Viral—host co-speciation history was evaluated by comparing the topologies of the viral and host trees by using Jane V4. Since there were only two lobe-finned fish and one shark species that contain FLERVs, analyses for these two lineages were not performed.

The host trees used in these analyses are published host trees 35 , 36 , 37 , The number of co-speciation events was calculated by using a genetic algorithm, with the number of generations, and population set to To assess the probability of observing the inferred number of co-speciation events by chance, the random tip mapping method implemented in Jane v4. The T estimates were directly inferred from those of their hosts 35 , 39 , 40 under the well-established FV-host co-speciation assumption 5 , 6 Table 2 , nodes I—IX. The model fitting was performed by using the lm function implemented in R 3.

The values of S and T were log-transformed base 10 prior to the linear model fitting. The model was then extrapolated to estimate the timescale of other nodes from their S estimates. This process was applied to all of the 7, posterior Bayesian phylogenies to obtain their full posterior distributions Fig. The immediate outgroup of the clade was used to root the tree.

FLERV lineages that consist of one sequence sample were excluded from analyses as ML ancestral reconstruction requires more than one sequence, unless samples from the same host genus but different species exist. In such cases, they would be grouped with the other FLERV lineage and their ancestor would be inferred together.

Their Pol protein aa phylogeny, together with those of extant mammalian FVs, was estimated by using MrBayes 3. The tree was rooted according to the tree in Fig. The position of the root was confirmed by using several Class III retroviruses as outgroups. All data used in this study are available from the authors upon request. How to cite this article: Aiewsakun, P. Marine origin of retroviruses in the early Palaeozoic Era.

The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript. We thank members of the research group for constructive comments and discussions. The authors declare no competing financial interests. Author contributions P. National Center for Biotechnology Information , U. Nat Commun. Published online Jan Pakorn Aiewsakun 1 and Aris Katzourakis a, 1. Author information Article notes Copyright and License information Disclaimer. Received May 13; Accepted Nov This work is licensed under a Creative Commons Attribution 4. This article has been cited by other articles in PMC.

Abstract Very little is known about the ancient origin of retroviruses, but owing to the discovery of their ancient endogenous viral counterparts, their early history is beginning to unfold. Results Discovery of FLERVs in amphibian and fish genomes By using tBLASTn and the reverse transcriptase RT protein of CoeEFV as a screening probe, 1, RT sequences were retrieved from publically accessible nucleotide GenBank databases, including the database of GenBank non-redundant nucleotide sequences, expressed sequence tags, high throughput genomic sequences, whole genome shotgun sequences and transcriptome shotgun assembly sequences.

Natural History Timeline PART I: PALEOZOIC: From the Cambrian explosion to the Great Dying

Open in a separate window. Figure 1. Figure 2. Figure 3. Evolutionary timescale of FLERVs Studies have shown that the rate estimates of mammalian FV evolution are time dependent 16 , 18 , and that this time-dependent rate phenomenon TDRP can be empirically described well by a power-law decay function Figure 4.

Discussion Here we report 36 lineages of novel FLERVs residing in the genomes of salamanders, a frog, ray-finned fish, lobe-finned fish and shark Table 1 , see also Supplementary Table 1. Phylogenetic analyses To investigate phylogenetic relationships between FVs and FLERVs in more detail, we estimated their phylogeny based on a manually curated Pol protein alignment aa.

Co-speciation analyses Viral—host co-speciation history was evaluated by comparing the topologies of the viral and host trees by using Jane V4. Data availability All data used in this study are available from the authors upon request. Additional information How to cite this article: Aiewsakun, P. Peer Review File: Click here to view. Acknowledgments P. Footnotes The authors declare no competing financial interests. References Hayward A. Pan-vertebrate comparative genomics unmasks retrovirus macroevolution. USA , — Retroviral diversity and distribution in vertebrates.

Endogenous viruses: connecting recent and ancient viral evolution. Virology — , 26—37 Identification of an ancient endogenous retrovirus, predating the divergence of the placental mammals. Macroevolution of complex retroviruses. Science , Discovery of prosimian and afrotherian foamy viruses and potential cross species transmissions amidst stable and ancient mammalian co-evolution.

Retrovirology 11 , 61 A molecular timescale for vertebrate evolution. Nature , — A molecular timescale of eukaryote evolution and the rise of complex multicellular life. BMC Evol. Uncertainty in the timing of origin of animals and the limits of precision in molecular timescales. An endogenous foamy virus in the aye-aye Daubentonia madagascariensis. Endogenous viral sequences from the Cape golden mole Chrysochloris asiatica reveal the presence of foamy viruses in all major placental mammal clades. An endogenous foamy-like viral element in the coelacanth genome.

PLoS Pathog. The genome of the platyfish, Xiphophorus maculatus , provides insights into evolutionary adaptation and several complex traits. Network dynamics of eukaryotic LTR retroelements beyond phylogenetic trees. Time-dependent rate phenomenon in viruses. Time dependency of foamy virus evolutionary rate estimates.

Analyses of evolutionary dynamics in viruses are hindered by a time-dependent bias in rate estimates. The impact of calibration and clock-model choice on molecular estimates of divergence times. DNA transposons: nature and applications in genomics. Genomics 11 , — Discovery and analysis of the first endogenous lentivirus.

Natl Acad. Relative rates of nucleotide substitution in frogs. Molecular characterization of the HIV type 1 subtype C accessory genes vif , vpr , and vpu. AIDS Res. Retroviruses 23 , — Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. On the estimation of the insertion time of LTR retrotransposable elements.

Ancient co-speciation of simian foamy viruses and primates. Oldest coelacanth, from the early Devonian of Australia. Multi-locus phylogenetic analysis reveals the pattern and tempo of bony fish evolution. PLoS Curr. Tree Life 5 , doi:; DOI: Interrelationships of basal synapsids: cranial and postcranial morphological partitions suggest different topologies.

Paleozoic origin of insect large dsDNA viruses. The ornamentation of the head-shield is composed of coarse-granular tubercles Fig 5A—5C. Platylomaspis is more comparable to Gumuaspis in the pear-shaped head-shield, short rostral process, and leaf-shaped inner corners. Platylomaspis differs from Gumuaspis mainly by its much broader ventral rim, much larger inner corner, and less branchial fossae. In addition, the lateral margin of the dorsal head-shield is smooth in Gumuaspis , but serrated in Platylomaspis. The ornamentation of head-shield is composed of stellate tubercles in Gumuaspis in contrast to coarse-granular tubercles in Platylomaspis Figs 2A , 3 and 4.

Nanningaspis resembles Gumuaspis and Platylomaspis in bearing a pear-shaped head-shield with a rod-like rostral process and without laterally projecting corner Figs 2A and 3 —5. In comparison to Gumuaspis , Nanningaspis is more similar to Platylomaspis in having a broad ventral rim and coarse-granular tubercles. Nanningaspis differs from Platylomaspis in having over two times larger sized head-shield Figs 3 — 5. Galeaspids display little size variation, e. In addition, the lateral margin of the head-shield is serrated in Platylomaspis , but smooth in Nanningaspis.

Although the median dorsal opening, orbital opening, and sensory canal system remain unclear in both taxa, the available information indicates that the orbital opening of Nanningaspis is more laterally set than that of Platylomaspis , and probably faces anterolaterally Figs 3 — 5. To explore the phylogenetic positions of Platylomaspis and Nanningaspis , we conducted phylogenetic analysis using the dataset of Zhu and Gai [ 4 ] with the addition of Character 54, broad ventral rim: absent 0 , present 1 S1 File.

The character data entry and formatting were performed in Mesquite version 3. All characters were treated as unordered and weighted equally, as in the earlier versions of this dataset. A basal osteostracan Ateleaspis is selected as outgroup for the phylogenetic analysis. The analysis was conducted using PAUP 4. These three equally most-parsimonious trees differ only in the positions of 3 Silurian genera Hanyangaspis , Changxingaspis and Dayongaspis and yield three major clades as defined in earlier works, namely the Eugaleaspiformes, Polybranchiaspiformes and Huananaspiformes.

Platylomaspis and Nanningaspis fall into the Polybranchiaspiformes. Within Polybranchiaspiformes, Platylomaspis is resolved as the sister group of Nanningaspis by the synapomorphy of the broad ventral rim. They are consistently clustered with Gumuaspis to form a monophyletic group, Gumuaspidae fam. Our phylogenetic analysis indicates that the Gumuaspidae occupies the most basal position of Polybranchiaspiformes.

The Polybranchiaspiformes is a highly diverse group of galeaspids, which was assumed to occur from the Lochkovian to the Eifelian [ 4 , 47 ]. The earliest fossil record of Polybrachiaspifomes was from the Xishancun Formation Lochkovian including Pentathraspis , Polybranchiaspis , Laxaspis , Damaspis , Pseudolaxaspis , Diandongaspis , and Altigibbaspis [ 43 , 48 — 51 ]. The high diversity of Polybrachiaspifomes in the Xishancun Formation indicated that the Polybrachiaspifomes should have differentiated earlier. By the Pragian, the diversity of Polybranchiaspiformes suddenly declined.

Except for the Gumuaspidae, there are only two unusually large-sized polybranchiaspiforms: Bannhuanaspis vukhuci from the uppermost part of the late Lochkovian to the early Pragian Si Ka Formation of Bac Bo, Vietnam and Dongfangaspis major from the Pragian Pingyipu Formation of Sichuan survived [ 43 , 52 ].

The findings of Platylomaspis and Nanningaspis also have important palaeobiogeographic significance. For the Galeaspida, a correlation between phylogeny and palaeobiogeography is observed, e. Over the last decades, the polybranchiaspiforms have been assumed to be endemic to southern China and northern Vietnam, never found in Tarim [ 4 , 47 ].

As galeaspids are heavily armoured bottom-dwellers with limited locomotory and dispersal capabilities, the continents and open oceans became the major obstacles for their migration and dispersal [ 53 , 54 ]. Geological and paleontological evidence indicates that the South China, the North China and the Tarim blocks were very close during the Llandovery of Silurian.

The finding of Platylomaspis in Tarim and Nanningaspis in Guangxi corroborates that a united Tarim-South China Block existed in the Llandovery and Wenlock of Silurian [ 18 , 20 , 54 ], and provides a potential route for early polybranchiaspiforms migrating from the Tarim Block to the South China Block. The united block was probably divided into two blocks in the Ludlow or later, when the Tarim Block began to drift away to the northwest [ 18 ].

Platylomaspis and Nanningaspis are characterized by a pear-shaped head-shield with a rostral process and a unique broad ham-brim-like ventral rim. The rostral process, which was regarded as a diagnostic character of Huananaspiformes [ 55 ] are also present in other two major groups of galeaspids, e. Gumuaspidae in Polybranchiaspiformes, Eugaleaspidae in Eugaleaspiformes [ 44 , 56 ].

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The rostrum of galeaspids might have the same functions as the rostrum of other agnathans that lived under similar environmental conditions, e. It may have a sensory function in search of food or a hydrodynamic function [ 60 , 61 ]. However, the hypothesis of the protective function of the rostrum by scaring predators in osteotracans proposed by Janvier [ 62 ] are probably not applicable to Gumuaspidae as it lacks other processes, e.

The recurrent evolution of similar rostral processes in various agnathan groups probably indicates similar ecological pressures upon the clades and diversifications into comparable niches [ 63 ].

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The wide-brimmed head-shield is a diagnostic character uniquely shared by Platylomaspis and Nanningaspis Fig 8A. The morphological adaptations of galeaspids, e. Like modern Cottidae and Gobiesocidae, the strongly armored and flattened head-shield of galeaspids provides greater density and helps the fish maintain contact with the substratum in moderate currents without a significant energetic cost [ 9 , 64 ]. Therefore, the extreme flattening of the head-shields strengthened by the wide ventral rim in Platylomaspis and Nanningaspis at least can help them better adapt to the benthic habitat or have a selective advantage when living in an environment dominated by strong currents.

Here, we further show that the wide-brimmed head-shield with a rod-like rostral process in Platylomaspis and Nanningaspis is probably analogous to the pectoral disc and long duck-billed snout in modern rays Fig 9 , e. Dasyatis and Rajella [ 65 ]. The head shape of the latter facilitates them to burrow underneath the sands in order to avoid predators and wait for feeding opportunities.

A 1 —C 1 , in dorsal view; A 2 —C 2 , a cross section through the head-shield at the level indicated by the line in A 1 —C 1. Abbreviations: br. Galeaspids have a remarkable character combination to make breathing and feeding more effective. Like modern rays, galeaspids have their mouth and gill openings on the ventral side of head-shield Fig 9B , m, br.

The synchrotron radiation X-ray tomographic study revealed that the large median dorsal opening penetrated the roof of oral cavity to communicate with the oral cavity and served for the main water intake device [ 1 ]. The diagnostic median dorsal opening of galeaspids is probably analogous to the spiracle in modern rays Fig 9C , spi through which the oxygenated water is inhaled. After oxygen is exchanged in gills, the deoxygenated water is exhaled though the ventral branchial opening. This is a useful adaptation for a benthic animal because it can respire oxygen without any need to move and have its mouth free for feeding.

Abbreviations: ad. However, this hypothesis of the partial burrowing habit is not suitable for most galeaspids because their median dorsal openings are so subterminal, or even terminal, that the silt and mud would pour into oralobranchial chamber when they were buried to inhale water Fig 8B. Being choked while hiding in sands means that the galeaspids cannot hide themselves in sands and are subject to the danger of predators.

By contrast, the wide-brimmed head-shield and rostral process in Platylomaspis and Nanningaspis had set the median dorsal opening and orbital openings highly in the middle of the head-shield, which not only makes the head-shield easy to be buried in silt or mud, but also can keep eyes and the large median dorsal opening outside for vision and respiration Fig 10E and 10F. In this case, the rostral process could possibly function as a detector of potential food in silt or mud like the long duck-billed snout of modern rays.

In addition, the coarse ornamentation and serrated lateral margin in Platylomaspis would play a role in resisting the tendency to slide backwards while moving forward through the sediment as proposed in some ctenaspid heterostracans sl. Hence, we propose that the unique wide-brimmed head-shield together with the rostral process in Platylomaspis and Nanningaspis is most likely to be a special adaptation for a semi-infaunal benthos, representing a partial burrowing habit in galaeaspids.

With the semi-infaunal habit, Platylomaspis and Nanningaspis were better hidden from predators than epifaunal galeaspids and could stay in moderate currents with less energetic cost. Recent studies indicated that the ventral rim of galeaspids had undergone an opposite modification in the Gantarostrataspidae [ 9 ], a clade of Huananaspiformes. Compared to the very broad ventral rim in Platylomaspis and Nanningaspis , the ventral rim of the Gantarostrataspidae is largely reduced, and even completely lost to form a streamlined torpedo-like head-shield Fig 8C to minimize the water drag by reducing the magnitude of the pressure gradient over the body [ 9 ].

Ordovician fish spines from Girvan, Scotland

This indicates that some galeaspids such as Rhegmaspis probably became more effective swimmer for a suprabenthic or nektonic habit Fig 11 , up. As such, the long rostral process was probably used as a scraper to plow the bottom in a relatively high speed to stir digestible materials for a more efficient filtering than the epibenthic galeaspids [ 9 ]. The discoveries of Nanningaspis from the Nakaolin Formation, Dongfangaspis from the Pingyipu Formation, and Rhegmaspis from the Posongchong Formation indicate that the demersal galeaspids had further developed three different kinds of habit types: semi-infaunal benthic half buried Fig 10 bottom , epibenthic Fig 11 , middle , and suprabenthic nektonic Fig 11 , up habits to occupy different vertical ecological niches by the Pragian of the Early Devonian.

Coupled with such a habit differentiation, galeaspids reached the peak of their diversity during the Pragian[ 69 ]. Bottom: Nanningaspis lived in a semi-infaunal benthic half buried habit; middle: Dongfangaspis lived in a epibenthic habit; up: Rhegmaspis lived in a suprabenthic nektonic habit. Browse Subject Areas? Click through the PLOS taxonomy to find articles in your field. Materials and methods Materials The material of Platylomaspis serratus gen.

Geological settings Platylomaspis gen. Download: PPT. Fig 1. Fish localities and lithological columns of the fish-bearing stratigraphy. Methods All the materials were prepared mechanically using a vibro tool with a tungsten-carbide bit or a needle, and some specimens were reversed on latex casts. Nomenclatural acts The electronic edition of this article conforms to the requirements of the amended International Code of Zoological Nomenclature, and hence the new names contained herein are available under that Code from the electronic edition of this article.

Type genus. Gumuaspis Wang et Wang, Referred genera. Fig 3. Photograph of Platylomaspis serratus gen. Fig 4. The restoration of Platylomaspis serratus gen. Fig 5. Photograph and restoration of Nanningaspis zengi gen. Descriptions Platylomaspis serratus. Nanningaspis zengi. Comparisons Platylomaspis is more comparable to Gumuaspis in the pear-shaped head-shield, short rostral process, and leaf-shaped inner corners. Phylogenetic results To explore the phylogenetic positions of Platylomaspis and Nanningaspis , we conducted phylogenetic analysis using the dataset of Zhu and Gai [ 4 ] with the addition of Character 54, broad ventral rim: absent 0 , present 1 S1 File.

Fig 6. Strict consensus of 3 maximum parsimony trees resulted from the present analysis. Discussion Temporal and palaeobiogeographic distribution of Polybranchiaspiformes Our phylogenetic analysis indicates that the Gumuaspidae occupies the most basal position of Polybranchiaspiformes. Fig 7. A phylogenetic tree of galeaspid families projected against stratigraphy. Ecomorphological implications Platylomaspis and Nanningaspis are characterized by a pear-shaped head-shield with a rostral process and a unique broad ham-brim-like ventral rim.

Fig 8. The modification of the ventral rim in galeaspids illustrated by Dinghua Yang. Fig 9. The morphological convergence between galeaspids and morden rays probably for the half burrowing habit. Fig Adaptions of the water intake device in the half burrowing fishes. Ecological restoration of galeapids during the Pragian showing three different types of habits illustrated by Dinghua Yang. Supporting information. S1 File. The nexus file of the data matrix with 41 ingroup taxa and 54 characters. S2 File. The log file of the phylogenetic analysis. References 1. Fossil jawless fish from China foreshadows early jawed vertebrate anatomy.

Gai ZK, Zhu M.


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