Molecular fossils illuminate the evolution of retroviruses following a macroevolutionary transition from land to water

The ancestor of cetaceans underwent a macroevolutionary transition from land to water early in the Eocene Period >50 million years ago. However, little is known about how diverse retroviruses evolved during this shift from terrestrial to aquatic environments. Did retroviruses transition into water accompanying their hosts? Did retroviruses infect cetaceans through cross-species transmission after cetaceans invaded the aquatic environments? Endogenous retroviruses (ERVs) provide important molecular fossils for tracing the evolution of retroviruses during this macroevolutionary transition. Here, we use a phylogenomic approach to study the origin and evolution of ERVs in cetaceans. We identify a total of 8,724 ERVs within the genomes of 25 cetaceans, and phylogenetic analyses suggest these ERVs cluster into 315 independent lineages, each of which represents one or more independent endogenization events. We find that cetacean ERVs originated through two possible routes. 298 ERV lineages may derive from retrovirus endogenization that occurred before or during the transition from land to water of cetaceans, and most of these cetacean ERVs were reaching evolutionary dead-ends. 17 ERV lineages are likely to arise from independent retrovirus endogenization events that occurred after the split of mysticetes and odontocetes, indicating that diverse retroviruses infected cetaceans through cross-species transmission from non-cetacean mammals after the transition to aquatic life of cetaceans. Both integration time and synteny analyses support the recent or ongoing activity of multiple retroviral lineages in cetaceans, some of which proliferated into hundreds of copies within the host genomes. Although ERVs only recorded a proportion of past retroviral infections, our findings illuminate the complex evolution of retroviruses during one of the most marked macroevolutionary transitions in vertebrate history.     

A comparative study of body size and clutch size across the parasitoid Hymenoptera

Across animal species, body size and clutch size often form part of a suite of associated life history traits, exemplified by the "fast-slow continuum" in mammals. Across the parasitoid Hymenoptera however, a major axis of life history variation is the development mode of the larva (koinobiosis versus idiobiosis), and body size and clutch size do not seem to form clear associations with this major axis. Here we use a large comparative data set and the latest phylogenetic information to explore hypotheses that might explain the variation in body size and clutch size across species in parasitoids. We find evidence for three novel evolutionary correlations: changes in the stage of host attacked by the parasitoid (i.e. egg, larva, pupa) significantly predict changes in both body size and clutch size, whilst in gregarious species changes to higher latitudes are associated with reduced clutch size. We also find a number of hypothesized cross-species (phenotypic) associations that, however, we cannot demonstrate are the result of evolutionary correlations: large bodied species in our data tend to lay small clutches; koinobionts are larger than idiobionts attacking the same host stage; tropical species are smaller than temperate species (Bergmann's rule). Our results provide support for theoretical models of trait evolution in parasitoids, whilst the associations between latitude and life history may help explain why species richness in the family Ichneumonidae peaks at intermediate latitudes. Our results also show the continuing value of phylogenetically-based comparative analyses and demonstrate that recent work on parasitoid phylogenetics has produced significant benefits for our understanding of life history evolution.     

Why are some species more commonly afflicted by arthritis than others? A comparative study of spondyloarthropathy in primates and carnivores

Spondyloarthropathy is a painful arthritic affliction of humans that also occurs in wild mammals. Important questions remain concerning the underlying causes of spondyloarthropathy in mammals, particularly regarding whether it is infectious in origin or driven by genetic predisposition and environmental stressors. Moreover, spondyloarthropathy has negative effects on host fitness, leading to potential conservation concerns if it impacts threatened species. Using a comparative data set on the prevalence of joint disease in 34 primate species and 100 carnivore species, we tested predictions involving the epidemiological correlates of spondyloarthropathy in wild mammals. Analyses revealed that 5.6% of primates and 3.6% of carnivores exhibited signs of spondyloarthropathy, with maximum incidence as high as 22% in great apes and 27% in bears. We tested whether prevalence of spondyloarthropathy increases with population density and group size, greater contact with soil, a slower host life history, increased ranging, dietary factors and body mass. We found general support for an effect of body mass, with larger bodied primates and carnivores exhibiting a higher prevalence of spondyloarthropathy. In addition, more threatened species experienced higher rates of spondyloarthropathy, with this association influenced by body mass and phylogeny. The effect of body mass could reflect that larger animals are exposed to more pathogens through greater consumption of resources, or that joints of larger bodied mammals experience greater biomechanical stresses, resulting in inflammation and activation of local joint infections.     

Studies of endogenous retroviruses reveal a continuing evolutionary saga

Retroviral replication involves the formation of a DNA provirus integrated into the host genome. Through this process, retroviruses can colonize the germ line to form endogenous retroviruses (ERVs). ERV inheritance can have multiple adverse consequences for the host, some resembling those resulting from exogenous retrovirus infection but others arising by mechanisms unique to ERVs. Inherited retroviruses can also confer benefits on the host. To meet the different threats posed by endogenous and exogenous retroviruses, various host defences have arisen during evolution, acting at various stages on the retrovirus life cycle. In this Review, I describe our current understanding of the distribution and architecture of ERVs, the consequences of their acquisition for the host and the emerging details of the intimate evolutionary relationship between virus and vertebrate host.     

Phylogenetic Analysis Reveals That ERVs "Die Young" but HERV-H Is Unusually Conserved

About 8% of the human genome is made up of endogenous retroviruses (ERVs). Though most human endogenous retroviruses (HERVs) are thought to be irrelevant to our biology notable exceptions include members of the HERV-H family that are necessary for the correct functioning of stem cells. ERVs are commonly found in two forms, the full-length proviral form, and the more numerous solo-LTR form, thought to result from homologous recombination events. Here we introduce a phylogenetic framework to study ERV insertion and solo-LTR formation. We then apply the framework to site patterns sampled from a set of long alignments covering six primate genomes. Studying six categories of ERVs we quantitatively recapitulate patterns of insertional activity that are usually described in qualitative terms in the literature. A slowdown in most ERV groups is observed but we suggest that HERV-K activity may have increased in humans since they diverged from chimpanzees. We find that the rate of solo-LTR formation decreases rapidly as a function of ERV age and that an age dependent model of solo-LTR formation describes the history of ERVs more accurately than the commonly used exponential decay model. We also demonstrate that HERV-H loci are markedly less likely to form solo-LTRs than ERVs from other families. We conclude that the slower dynamics of HERV-H suggest a host role for the internal regions of these exapted elements and posit that in future it will be possible to use the relationship between full-length proviruses and solo-LTRs to help identify large scale co-options in distant vertebrate genomes.     

Life history evolution and cellular mechanisms associated with increased size in high‐altitude Drosophila

Understanding the physiological and genetic basis of growth and body size variation has wide‐ranging implications, from cancer and metabolic disease to the genetics of complex traits. We examined the evolution of body and wing size in high‐altitude Drosophila melanogaster from Ethiopia, flies with larger size than any previously known population. Specifically, we sought to identify life history characteristics and cellular mechanisms that may have facilitated size evolution. We found that the large‐bodied Ethiopian flies laid significantly fewer but larger eggs relative to lowland, smaller‐bodied Zambian flies. The highland flies were found to achieve larger size in a similar developmental period, potentially aided by a reproductive strategy favoring greater provisioning of fewer offspring. At the cellular level, cell proliferation was a strong contributor to wing size evolution, but both thorax and wing size increases involved important changes in cell size. Nuclear size measurements were consistent with elevated somatic ploidy as an important mechanism of body size evolution. We discuss the significance of these results for the genetic basis of evolutionary changes in body and wing size in Ethiopian D. melanogaster.     

A New Approach to Establish a Cell Line with Reduced Risk of Endogenous Retroviruses

Endogenous retroviruses (ERVs) are integrated as DNA proviruses in the genomes of all mammalian species. Several ERVs are replication-competent and produced as fully infectious viruses from host cell. Thus, live-attenuated vaccines and biological substances have been prepared using the cell lines which may produce ERV. Indeed, we recently reported that several commercial live-attenuated vaccines for pets were contaminated with the infectious feline endogenous retrovirus, RD-114. In this study, to establish a cell line for vaccine manufacture with reduced risk of ERVs, we generated a cell line stably expressing human tetherin (Teth-CRFK cells). The release of infectious ERV from Teth-CRFK cells was suppressed to undetectable levels, while the production of parvovirus in Teth-CRFK cells was similar to that in parental CRFK cells. These observations suggest that Teth-CRFK cells will be useful as a cell line for the manufacture of live-attenuated vaccines or biological substances with reduced risk of ERV.     

The evolutionary dynamics of endogenous retroviruses

Endogenous retroviruses (ERVs) are vertically transmitted intragenomic elements derived from integrated retroviruses. ERVs can proliferate within the genome of their host until they either acquire inactivating mutations or are lost by recombinational deletion. We present a model that unifies current knowledge of ERV biology into a single evolutionary framework. The model predicts the possible long-term outcomes of retroviral germline infection and can account for the variable patterns of observed ERV genetic diversity. We hope the model will provide a useful framework for understanding ERV evolution, enabling the testing of evolutionary hypotheses and the estimation of parameters governing ERV proliferation.     

Host traits and parasite species richness in even and odd-toed hoofed mammals, Artiodactyla and Perissodactyla

Host social, ecological and life history traits are predicted to influence both parasite establishment within host species and the distribution of parasites among host species. Yet only a few studies have investigated the role multiple host traits play in determining patterns of infection across diverse parasite groups. To explore the association between host traits and parasite species richness (PSR), we assembled a comprehensive database encompassing 601 parasites (including viruses, bacteria, protozoa, helminths and arthropods) reported to infect 96 species from two well-studied and diverse host clades: even- and odd-toed hoofed mammals (Artiodactyla and Perissodactyla). Comparative analyses were used to examine associations between three sets of host variables (life history and body mass, social and mating behavior, and ecological traits) and PSR for all parasites combined and for distinct parasite sub-groups. Results from a combination of phylogenetic and non-phylogenetic tests showed that PSR increased with host body size across all parasites groups. Counter to expectations, measures of parasite diversity decreased with host longevity and social group size, and associations between group size and PSR further depended on the underlying mating system of the host species. Our results suggest that body mass, longevity, and social organization influence the diversity and types of parasites reported to infect wild populations of hoofed mammals, and that multiple host and parasite traits can combine in unexpected ways to shape observed patterns.     

Cross-Species Transmission and Differential Fate of an Endogenous Retrovirus in Three Mammal Lineages

Endogenous retroviruses (ERVs) arise from retroviruses chromosomally integrated in the host germline. ERVs are common in vertebrate genomes and provide a valuable fossil record of past retroviral infections to investigate the biology and evolution of retroviruses over a deep time scale, including cross-species transmission events. Here we took advantage of a catalog of ERVs we recently produced for the bat Myotis lucifugus to seek evidence for infiltration of these retroviruses in other mammalian species (>100) currently represented in the genome sequence database. We provide multiple lines of evidence for the cross-ordinal transmission of a gammaretrovirus endogenized independently in the lineages of vespertilionid bats, felid cats and pangolin ~13–25 million years ago. Following its initial introduction, the ERV amplified extensively in parallel in both bat and cat lineages, generating hundreds of species-specific insertions throughout evolution. However, despite being derived from the same viral species, phylogenetic and selection analyses suggest that the ERV experienced different amplification dynamics in the two mammalian lineages. In the cat lineage, the ERV appears to have expanded primarily by retrotransposition of a single proviral progenitor that lost infectious capacity shortly after endogenization. In the bat lineage, the ERV followed a more complex path of germline invasion characterized by both retrotransposition and multiple infection events. The results also suggest that some of the bat ERVs have maintained infectious capacity for extended period of time and may be still infectious today. This study provides one of the most rigorously documented cases of cross-ordinal transmission of a mammalian retrovirus. It also illustrates how the same retrovirus species has transitioned multiple times from an infectious pathogen to a genomic parasite (i.e. retrotransposon), yet experiencing different invasion dynamics in different mammalian hosts.     

Species traits and environmental characteristics together regulate ant‐associated biodiversity

Host‐associated organisms (e.g., parasites, commensals, and mutualists) may rely on their hosts for only a portion of their life cycle. The life‐history traits and physiology of hosts are well‐known determinants of the biodiversity of their associated organisms. The environmental context may strongly influence this interaction, but the relative roles of host traits and the environment are poorly known for host‐associated communities. We studied the roles of host traits and environmental characteristics affecting ant‐associated mites in semi‐natural constructed grasslands in agricultural landscapes of the Midwest USA. Mites are frequently found in ant nests and also riding on ants in a commensal dispersal relationship known as phoresy. During nonphoretic stages of their development, ant‐associated mites rely on soil or nest resources, which may vary depending on host traits and the environmental context of the colony. We hypothesized that mite diversity is determined by availability of suitable host ant species, soil detrital resources and texture, and habitat disturbance. Results showed that that large‐bodied and widely distributed ant species within grasslands support the most diverse mite assemblages. Mite richness and abundance were predicted by overall ant richness and grassland area, but host traits and environmental predictors varied among ant hosts: mites associated with Aphaenogaster rudis depended on litter depth, while Myrmica americana associates were predicted by host frequency and grassland age. Multivariate ordinations of mite community composition constructed with host ant species as predictors demonstrated host specialization at both the ant species and genus levels, while ordinations with environmental variables showed that ant richness, soil texture, and grassland age also contributed to mite community structure. Our results demonstrate that large‐bodied, locally abundant, and cosmopolitan ant species are especially important regulators of phoretic mite diversity and that their role as hosts is also dependent on the context of the interaction, especially soil resources, texture, site age, and area.     

Encephalization and the evolution of longevity in mammals

Allometric principles account for most of the observed variation in maximum life span among mammals. When body-size effects are controlled for, most of the residual variance in mammalian life span can be explained by variations in brain size, metabolic rate and body temperature. It is shown that species with large brains for a given body size and metabolic rate, such as anthropoid primates, also have long maximum life spans. Conversely, mammals with relatively high metabolic rates and low levels of encephalization, as in most insectivores and rodents, tend to have short life spans. The hypothesis is put forward that encephalization and metabolic rate, which may govern other life history traits, such as growth and reproduction, are the primary determinants directing the evolution of mammalian longevity.     

Local host-tick coextinction in neotropical forest fragments

Ticks are obligatory parasites with complex life cycles that often depend on larger bodied vertebrates as final hosts. These traits make them particularly sensitive to local coextinction with their host. Loss of wildlife abundance and diversity should thus lead to loss of tick abundance and diversity to the point where only generalist tick species remain. However, direct empirical tests of these hypotheses are lacking, despite their relevance to our understanding of tick-borne disease emergence in disturbed environments. Here, we compare vertebrate and tick communities across 12 forest islands and peninsulas in the Panama Canal that ranged 1000-fold in size (2.6–2811.3?ha). We used drag sampling and camera trapping to directly assess the abundance and diversity of communities of questing ticks and vertebrate hosts. We found that the abundance and species richness of ticks were positively related to those of wildlife. Specialist tick species were only present in fragments where their final hosts were found. Further, less diverse tick communities had a higher relative abundance of the generalist tick species Amblyomma oblongoguttatum, a potential vector of spotted fever group rickettsiosis. These findings support the host-parasite coextinction hypothesis, and indicate that loss of wildlife can indeed have cascading effects on tick communities. Our results also imply that opportunities for pathogen transmission via generalist ticks may be higher in habitats with degraded tick communities. If these patterns are general, then tick identities and abundances serve as useful bioindicators of ecosystem health, with low tick diversity reflecting low wildlife diversity and a potentially elevated risk of interspecific disease transmission via remaining host species and generalist ticks.     

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.     

Population differences in host use by a seed-beetle: local adaptation, phenotypic plasticity and maternal effects

For insects that develop inside discrete hosts, both host size and host quality constrain offspring growth, influencing the evolution of body size and life history traits. Using a two-generation common garden experiment, we quantified the contribution of maternal and rearing hosts to differences in growth and life history traits between populations of the seed-feeding beetle Stator limbatus that use a large-seeded host, Acacia greggii, and a small-seeded host, Pseudosamanea guachapele. Populations differed genetically for all traits when beetles were raised in a common garden. Contrary to expectations from the local adaptation hypothesis, beetles from all populations were larger, developed faster and had higher survivorship when reared on seeds of A. greggii (the larger host), irrespective of their native host. We observed two host plant-mediated maternal effects: offspring matured sooner, regardless of their rearing host, when their mothers were reared on P. guachapele (this was not caused by an effect of rearing host on egg size), and females laid larger eggs on P. guachapele. This is the first study to document plasticity by S. limbatus in response to P. guachapele, suggesting that plasticity is an ancestral trait in S. limbatus that likely plays an important role in diet expansion. Although differences between populations in growth and life history traits are likely adaptations to their host plants, host-associated maternal effects, partly mediated by maternal egg size plasticity, influence growth and life history traits and likely play an important role in the evolution of the breadth of S. limbatus’ diet. More generally, phenotypic plasticity mediates the fitness consequences of using novel hosts, likely facilitating colonization of new hosts, but also buffering herbivores from selection post-colonization. Plasticity in response to novel versus normal hosts varied among our study populations such that disentangling the historical role of plasticity in mediating diet evolution requires the consideration of evolutionary history.     

Life history evolution in cichlids 2: directional evolution of the trade-off between egg number and egg size

The negative relationship between offspring number and offspring size provides a classic example of the role of trade-offs in life history theory. However, the evolutionary transitions in egg size and clutch size that have produced this negative relationship are still largely unknown. Since body size may affect both of these traits, it would be helpful to understand how evolutionary changes in body size may have facilitated or constrained shifts in clutch and egg size. By using comparative methods with a database of life histories and a phylogeny of 222 genera of cichlid fishes, we investigated the order of evolutionary transitions in these traits in relation to each other. We found that the ancestral large-bodied cichlids first increased egg size, followed by a decrease in both body size and clutch size resulting in the common current combination of a small-bodied cichlid with a small clutch of large eggs. Furthermore, lineages that deviated from the negative relationship between clutch and egg size underwent different transitions in these traits according to their body size (large bodied genera have moved towards the large clutch/small egg end of the continuum and small bodied genera towards the small clutch/large egg end of the continuum) to reach the negative relationship between clutch size and egg size. Our results show that body size is highly important in shaping the negative relationship between clutch size and egg size.