Endogenous Viral Sequences from the Cape Golden Mole (Chrysochloris asiatica) Reveal the Presence of Foamy Viruses in All Major Placental Mammal Clades

Endogenous retroviruses provide important insights into the deep history of this viral lineage. Endogenous foamy viruses are thought to be very rare and only a few cases have been identified to date. Here we report a novel endogenous foamy virus (CaEFV) within the genome of the Cape golden mole (Chrysochloris asiatica). The identification of CaEFV reveals the presence of foamy virus in the placental mammal superorder Afrotheria. Phylogenetic analyses place CaEFV basal to other foamy viruses of Eutherian origin, suggesting an ancient codivergence between foamy virus and placental mammals. These findings have implications for understanding the long-term evolution, diversity, and biology of retroviruses.     

An Endogenous Foamy-like Viral Element in the Coelacanth Genome

Little is known about the origin and long-term evolutionary mode of retroviruses. Retroviruses can integrate into their hosts'' genomes, providing a molecular fossil record for studying their deep history. Here we report the discovery of an endogenous foamy virus-like element, which we designate ‘coelacanth endogenous foamy-like virus’ (CoeEFV), within the genome of the coelacanth (Latimeria chalumnae). Phylogenetic analyses place CoeEFV basal to all known foamy viruses, strongly suggesting an ancient ocean origin of this major retroviral lineage, which had previously been known to infect only land mammals. The discovery of CoeEFV reveals the presence of foamy-like viruses in species outside the Mammalia. We show that foamy-like viruses have likely codiverged with their vertebrate hosts for more than 407 million years and underwent an evolutionary transition from water to land with their vertebrate hosts. These findings suggest an ancient marine origin of retroviruses and have important implications in understanding foamy virus biology.     

The Extraordinary Evolutionary History of the Reticuloendotheliosis Viruses

The reticuloendotheliosis viruses (REVs) comprise several closely related amphotropic retroviruses isolated from birds. These viruses exhibit several highly unusual characteristics that have not so far been adequately explained, including their extremely close relationship to mammalian retroviruses, and their presence as endogenous sequences within the genomes of certain large DNA viruses. We present evidence for an iatrogenic origin of REVs that accounts for these phenomena. Firstly, we identify endogenous retroviral fossils in mammalian genomes that share a unique recombinant structure with REVs—unequivocally demonstrating that REVs derive directly from mammalian retroviruses. Secondly, through sequencing of archived REV isolates, we confirm that contaminated Plasmodium lophurae stocks have been the source of multiple REV outbreaks in experimentally infected birds. Finally, we show that both phylogenetic and historical evidence support a scenario wherein REVs originated as mammalian retroviruses that were accidentally introduced into avian hosts in the late 1930s, during experimental studies of P. lophurae, and subsequently integrated into the fowlpox virus (FWPV) and gallid herpesvirus type 2 (GHV-2) genomes, generating recombinant DNA viruses that now circulate in wild birds and poultry. Our findings provide a novel perspective on the origin and evolution of REV, and indicate that horizontal gene transfer between virus families can expand the impact of iatrogenic transmission events.     

Repeated invasions into the twilight zone: evolutionary origins of a novel assemblage of fishes from deep Caribbean reefs

Mesophotic and deeper reefs of the tropics are poorly known and underexplored ecosystems worldwide. Collectively referred to as the ‘twilight zone’, depths below ~30–50 m are home to many species of reef fishes that are absent from shallower depths, including many undescribed and endemic species. We currently lack even a basic understanding of the diversity and evolutionary origins of fishes on tropical mesophotic reefs. Recent submersible collections in the Caribbean have provided new specimens that are enabling phylogenetic reconstructions that incorporate deep‐reef representatives of tropical fish genera. Here, we investigate evolutionary depth transitions in the family Gobiidae (gobies), the most diverse group of tropical marine fishes. Using divergence‐time estimation coupled with stochastic character mapping to infer the timing of shallow‐to‐deep habitat transitions in gobies, we demonstrate at least four transitions from shallow to mesophotic depths. Habitat transitions occurred in two broad time periods (Miocene, Pliocene–Pleistocene), and may have been linked to the availability of underutilized niches, as well as the evolution of morphological/behavioural adaptations for life on deep reefs. Further, our analysis shows that at least three evolutionary lineages that invaded deep habitats subsequently underwent speciation, reflecting another unique mode of radiation within the Gobiidae. Lastly, we synthesize depth distributions for 95 species of Caribbean gobies, which reveal major bathymetric faunal breaks at the boundary between euphotic and mesophotic reefs. Ultimately, our study is the first rigorous investigation into the origin of Caribbean deep‐reef fishes and provides a framework for future studies that utilize rare, deep‐reef specimens.     

Hot crenarchaeal viruses reveal deep evolutionary connections

The discovery of archaeal viruses provides insights into the fundamental biochemistry and evolution of the Archaea. Recent studies have identified a wide diversity of archaeal viruses within the hot springs of Yellowstone National Park and other high-temperature environments worldwide. These viruses are often morphologically unique and code for genes with little similarity to other known genes in the biosphere, a characteristic that has complicated efforts to trace their evolutionary history. Comparative genomics combined with structural analysis indicate that spindle-shaped virus lineages might be unique to the Archaea, whereas other icosahedral viruses might share a common lineage with viruses of Bacteria and Eukarya. These studies provide insights into the evolutionary history of viruses in all three domains of life.     

Human RNA “Rumor” Viruses: the Search for Novel Human Retroviruses in Chronic Disease

Summary: Retroviruses are an important group of pathogens that cause a variety of diseases in humans and animals. Four human retroviruses are currently known, including human immunodeficiency virus type 1, which causes AIDS, and human T-lymphotropic virus type 1, which causes cancer and inflammatory disease. For many years, there have been sporadic reports of additional human retroviral infections, particularly in cancer and other chronic diseases. Unfortunately, many of these putative viruses remain unproven and controversial, and some retrovirologists have dismissed them as merely “human rumor viruses.” Work in this field was last reviewed in depth in 1984, and since then, the molecular techniques available for identifying and characterizing retroviruses have improved enormously in sensitivity. The advent of PCR in particular has dramatically enhanced our ability to detect novel viral sequences in human tissues. However, DNA amplification techniques have also increased the potential for false-positive detection due to contamination. In addition, the presence of many families of human endogenous retroviruses (HERVs) within our DNA can obstruct attempts to identify and validate novel human retroviruses. Here, we aim to bring together the data on “novel” retroviral infections in humans by critically examining the evidence for those putative viruses that have been linked with disease and the likelihood that they represent genuine human infections. We provide a background to the field and a discussion of potential confounding factors along with some technical guidelines. In addition, some of the difficulties associated with obtaining formal proof of causation for common or ubiquitous agents such as HERVs are discussed.     

Genome-Wide Characterization of Endogenous Retroviruses in the Bat Myotis lucifugus Reveals Recent and Diverse Infections

Bats are increasingly recognized as reservoir species for a variety of zoonotic viruses that pose severe threats to human health. While many RNA viruses have been identified in bats, little is known about bat retroviruses. Endogenous retroviruses (ERVs) represent genomic fossils of past retroviral infections and, thus, can inform us on the diversity and history of retroviruses that have infected a species lineage. Here, we took advantage of the availability of a high-quality genome assembly for the little brown bat, Myotis lucifugus, to systematically identify and analyze ERVs in this species. We mined an initial set of 362 potentially complete proviruses from the three main classes of ERVs, which were further resolved into 13 major families and 86 subfamilies by phylogenetic analysis. Consensus or representative sequences for each of the 86 subfamilies were then merged to the Repbase collection of known ERV/long terminal repeat (LTR) elements to annotate the retroviral complement of the bat genome. The results show that nearly 5% of the genome assembly is occupied by ERV-derived sequences, a quantity comparable to findings for other eutherian mammals. About one-fourth of these sequences belong to subfamilies newly identified in this study. Using two independent methods, intraelement LTR divergence and analysis of orthologous loci in two other bat species, we found that the vast majority of the potentially complete proviruses identified in M. lucifugus were integrated in the last ∼25 million years. All three major ERV classes include recently integrated proviruses, suggesting that a wide diversity of retroviruses is still circulating in Myotis bats.     

Retroviruses and the placenta

Retroviruses are often expressed in the placenta. Placental expression probably evolved to facilitate retroviral transmission from mother to offspring and from offspring to mother. In the process, the placenta became a site where retroviral genes were 'domesticated' to serve adaptive functions in the host, including the manipulation of maternal physiology for the benefit of the fetus. The evolutionary interplay between retroviruses and host defenses may have contributed to the remarkable diversity of form among mammalian placentas and to mechanisms of genomic imprinting.     

Patterns of nucleotide diversity in two species of Mimulus are affected by mating system and asymmetric introgression

The evolutionary transition from outcrossing to self-fertilization has far-reaching implications for patterns of intraspecific genetic diversity and the potential for speciation. Using DNA sequence variation at two nuclear loci, we examined the divergence history of two closely related species of Mimulus. To investigate the effects of mating system and introgressive hybridization on the outcrossing M. guttatus and the selfing M. nasutus, we inspected nucleotide diversity within and between natural populations spanning the species' geographic ranges. High sequence similarity among populations of the selfing M. nasutus points to a single evolutionary origin for the species. Consistent with their distinct mating systems, all genetic variation in M. nasutus is distributed among populations, whereas M. guttatus exhibits appreciable levels of nucleotide diversity within populations. Silent genetic diversity is extensive in M. guttatus (mean theta(sil)/site = 0.077) and greatly exceeds the predicted twofold elevation in neutral variation for outcrossers relative to selfers. The finding of several M. guttatus sequences that share complete identity with sequences from M. nasutus suggests that recent asymmetric introgression may have occurred. We argue that exceptionally high nucleotide diversity in M. guttatus is consistent with a long-term history of directional introgression from M. nasutus to M. guttatus throughout the divergence of these two species.     

Hitchhiking and the Population Genetic Structure of Avian Influenza Virus

Previous studies have revealed a major difference in the phylogenetic structure, extent of genetic diversity, and selection pressure between the surface glycoproteins and internal gene segments of avian influenza viruses (AIV) sampled from wild birds. However, what evolutionary processes are responsible for these strikingly different evolutionary patterns is unclear. To address this issue, we estimated the rate of evolutionary change and time of origin of each segment of AIV sampled globally. Strikingly, the internal segments of the sampled AIV strains possess common ancestors that existed less than 200 years ago. Similarly recent times of origin were observed for each of the individual subtypes within the HA, NA, and NS gene segments. Such a shallow history of genetic diversity suggests an evolutionary model in which the genetic structure of AIV is shaped by a combination of occasional selective sweeps in the HA and NA (and possibly NS) segments, coupled with transient genetic linkage to the internal gene segments.     

Host-switching by a vertically transmitted rhabdovirus in Drosophila

A diverse range of endosymbionts are found within the cells of animals. As these endosymbionts are normally vertically transmitted, we might expect their evolutionary history to be dominated by host-fidelity and cospeciation with the host. However, studies of bacterial endosymbionts have shown that while this is true for some mutualists, parasites often move horizontally between host lineages over evolutionary timescales. For the first time, to our knowledge, we have investigated whether this is also the case for vertically transmitted viruses. Here, we describe four new sigma viruses, a group of vertically transmitted rhabdoviruses previously known in Drosophila. Using sequence data from these new viruses, and the previously described sigma viruses, we show that they have switched between hosts during their evolutionary history. Our results suggest that sigma virus infections may be short-lived in a given host lineage, so that their long-term persistence relies on rare horizontal transmission events between hosts.     

What Does Virus Evolution Tell Us about Virus Origins?

Despite recent advances in our understanding of diverse aspects of virus evolution, particularly on the epidemiological scale, revealing the ultimate origins of viruses has proven to be a more intractable problem. Herein, I review some current ideas on the evolutionary origins of viruses and assess how well these theories accord with what we know about the evolution of contemporary viruses. I note the growing evidence for the theory that viruses arose before the last universal cellular ancestor (LUCA). This ancient origin theory is supported by the presence of capsid architectures that are conserved among diverse RNA and DNA viruses and by the strongly inverse relationship between genome size and mutation rate across all replication systems, such that pre-LUCA genomes were probably both small and highly error prone and hence RNA virus-like. I also highlight the advances that are needed to come to a better understanding of virus origins, most notably the ability to accurately infer deep evolutionary history from the phylogenetic analysis of conserved protein structures.     

A heuristic method to reconstruct the history of sequences subject to recombination

Summary Sequences subject to recombination and gene conversion defy phylogenetic analysis by traditional methods since their evolutionary history cannot be adequately summarized by a tree. This study investigates ways to describe their evolutionary history and proposes a method giving a partial reconstruction of this history. Multigene families, viruses, and alleles from within populations experience recombinations/gene conversions, so the questions studied here are relevant for a large body of data and the suggested solutions should be very practical. The method employed was implemented in a program, RecPars, written in C and was used to analyze nine retroviruses.     

Viral evolution in deep time: lentiviruses and mammals

Lentiviruses are a distinctive genus of retroviruses that cause chronic, persistent infections in mammals, including humans. The emergence of pandemic HIV type-1 (HIV-1) infection during the late 20th century shaped a view of lentiviruses as 'modern' viruses. However, recent research has revealed an entirely different perspective, elucidating aspects of an evolutionary relationship with mammals that extends across many millions of years. Such deep evolutionary history is likely to be typical of many host-virus systems, fundamentally underpinning their interactions in the present day. For this reason, establishing the deep history of virus and host interaction is key to developing a fully informed approach to tackling viral diseases. Here, I use the example of lentiviruses to illustrate how paleovirological, geographic and genetic calibrations allow observations of virus and host interaction across a wide range of temporal and spatial scales to be integrated into a coherent ecological and evolutionary framework.