Reticulate evolution: Detection and utility in the phylogenomics era.

Phylogenomics has enriched our understanding that the Tree of Life can have network-like or reticulate structures among some taxa and genes. Two non-vertical modes of evolution - hybridization/introgression and horizontal gene transfer - deviate from a strictly bifurcating tree model, causing non-treelike patterns. However, these reticulate processes can produce similar patterns to incomplete lineage sorting or recombination, potentially leading to ambiguity. Here, we present a brief overview of a phylogenomic workflow for inferring organismal histories and compare methods for distinguishing modes of reticulate evolution. We discuss how the timing of coalescent events can help disentangle introgression from incomplete lineage sorting and how horizontal gene transfer events can help determine the relative timing of speciation events. In doing so, we identify pitfalls of certain methods and discuss how to extend their utility across the Tree of Life. Workflows, methods, and future directions discussed herein underscore the need to embrace reticulate evolutionary patterns for understanding the timing and rates of evolutionary events, providing a clearer view of life's history.

A phylogeny-informed characterisation of global tetrapod traits addresses data gaps and biases.

Tetrapods (amphibians, reptiles, birds, and mammals) are model systems for global biodiversity science, but continuing data gaps, limited data standardisation, and ongoing flux in taxonomic nomenclature constrain integrative research on this group and potentially cause biased inference. We combined and harmonised taxonomic, spatial, phylogenetic, and attribute data with phylogeny-based multiple imputation to provide a comprehensive data resource (TetrapodTraits 1.0.0) that includes values, predictions, and sources for body size, activity time, micro- and macrohabitat, ecosystem, threat status, biogeography, insularity, environmental preferences, and human influence, for all 33,281 tetrapod species covered in recent fully sampled phylogenies. We assess gaps and biases across taxa and space, finding that shared data missing in attribute values increased with taxon-level completeness and richness across clades. Prediction of missing attribute values using multiple imputation revealed substantial changes in estimated macroecological patterns. These results highlight biases incurred by nonrandom missingness and strategies to best address them. While there is an obvious need for further data collection and updates, our phylogeny-informed database of tetrapod traits can support a more comprehensive representation of tetrapod species and their attributes in ecology, evolution, and conservation research.

A Systematic Review of the Distribution and Prevalence of Viruses Detected in the Peromyscus maniculatus Species Complex (Rodentia: Cricetidae).

The North American Deermouse, Peromyscus maniculatus, is one of the most widespread and abundant mammals on the continent. It is of public health interest as a known host of several viruses that are transmissible to humans and can cause illness, including the acute respiratory disease Hantavirus Pulmonary Syndrome (HPS). However, recent taxonomic studies indicate that P. maniculatus is a complex of multiple species, raising questions about how to identify and interpret three decades of hantavirus monitoring data. We conducted a systematic review investigating the prevalence and spatial distribution of viral taxa detected in wild populations allocated to P. maniculatus. From the 46 relevant studies published from 2000 to 2022, we extracted and analyzed spatial occurrence data to calculate weighted populational prevalences for hantaviruses. We found that detection efforts have been concentrated in the Western United States and Mexico with a focus on the spread of Sin Nombre virus, the primary causative agent of HPS. There are significant gaps in the existing literature both geographically and in regard to the types of hantaviruses being sampled. These results are significantly impacted by a recent taxonomic split of P. maniculatus into four species, which results in the relabeling of 92% of hantavirus observations. Considering the uncertain, and likely multiple, phylogenetic histories of these viral hosts should be a key emphasis of future modeling efforts.

Using archived and biocollection samples towards deciphering the DNA virus diversity associated with rodent species in the families cricetidae and heteromyidae.

Rodentia is the most speciose order of mammals, and they are known to harbor a wide range of viruses. Although there has been significant research on zoonotic viruses in rodents, research on the diversity of other viruses has been limited, especially for rodents in the families Cricetidae and Heteromyidae. In fecal and liver samples of nine species of rodents, we identify 346 distinct circular DNA viral genomes. Of these, a large portion are circular, single-stranded DNA viruses in the families Anelloviridae (n = 3), Circoviridae (n = 5), Genomoviridae (n = 7), Microviridae (n = 297), Naryaviridae (n = 4), Vilyaviridae (n = 15) and in the phylum Cressdnaviricota (n = 13) that cannot be assigned established families. We also identified two large bacteriophages of 36 and 50 kb that are part of the class Caudoviricetes. Some of these viruses are clearly those that infect rodents, however, most of these likely infect various organisms associated with rodents, their environment or their diet.

Genomics expands the mammalverse.

Diverse mammal genomes open a new portal to hidden aspects of evolutionary history.

Diverse DNA virus genomes identified in fecal samples of Mexican free-tailed bats (Tadarida brasiliensis) captured in Chiricahua Mountains of southeast Arizona (USA).

Bats (order Chiroptera) are some of the most abundant mammals on earth and their species ecology strongly influences zoonotic potential. While substantial research has been conducted on bat-associated viruses, particularly on those that can cause disease in humans and/or livestock, globally, limited research has focused on endemic bats in the USA. The southwest region of the US is of particular interest because of its high diversity of bat species. We identified 39 single-stranded DNA virus genomes in the feces of Mexican free-tailed bats (Tadarida brasiliensis) sampled in the Rucker Canyon (Chiricahua Mountains) of southeast Arizona (USA). Twenty-eight of these belong to the virus families Circoviridae (n = 6), Genomoviridae (n = 17), and Microviridae (n = 5). Eleven viruses cluster with other unclassified cressdnaviruses. Most of the viruses identified represent new species. Further research on identification of novel bat-associated cressdnaviruses and microviruses is needed to provide greater insights regarding their co-evolution and ecology relative to bats.

The macroevolutionary impact of recent and imminent mammal extinctions on Madagascar.

Many of Madagascar's unique species are threatened with extinction. However, the severity of recent and potential extinctions in a global evolutionary context is unquantified. Here, we compile a phylogenetic dataset for the complete non-marine mammalian biota of Madagascar and estimate natural rates of extinction, colonization, and speciation. We measure how long it would take to restore Madagascar's mammalian biodiversity under these rates, the "evolutionary return time" (ERT). At the time of human arrival there were approximately 250 species of mammals on Madagascar, resulting from 33 colonisation events (28 by bats), but at least 30 of these species have gone extinct since then. We show that the loss of currently threatened species would have a much deeper long-term impact than all the extinctions since human arrival. A return from current to pre-human diversity would take 1.6 million years (Myr) for bats, and 2.9 Myr for non-volant mammals. However, if species currently classified as threatened go extinct, the ERT rises to 2.9 Myr for bats and 23 Myr for non-volant mammals. Our results suggest that an extinction wave with deep evolutionary impact is imminent on Madagascar unless immediate conservation actions are taken.

A solution to the challenges of interdisciplinary aggregation and use of specimen-level trait data.

Understanding variation of traits within and among species through time and across space is central to many questions in biology. Many resources assemble species-level trait data, but the data and metadata underlying those trait measurements are often not reported. Here, we introduce FuTRES (Functional Trait Resource for Environmental Studies; pronounced few-tress), an online datastore and community resource for individual-level trait reporting that utilizes a semantic framework. FuTRES already stores millions of trait measurements for paleobiological, zooarchaeological, and modern specimens, with a current focus on mammals. We compare dynamically derived extant mammal species' body size measurements in FuTRES with summary values from other compilations, highlighting potential issues with simply reporting a single mean estimate. We then show that individual-level data improve estimates of body mass-including uncertainty-for zooarchaeological specimens. FuTRES facilitates trait data integration and discoverability, accelerating new research agendas, especially scaling from intra- to interspecific trait variability.

Discovery of three cycloviruses in fecal samples from silver-haired bats (Lasionycteris noctivagans) in Arizona (USA).

Bats harbour a diverse array of viruses, some of which are zoonotic, and are one of the most speciose groups of mammals on earth. As part of an ongoing bat-associated viral diversity research project, we identified three cycloviruses (family Circoviridae) in fecal samples of silver-haired bats (Lasionycteris noctivagans) caught in Cave Creek Canyon of Arizona (USA). Two of the three identified genomes represent two new species in the genus Cyclovirus. Cycloviruses have been found in a wide range of environments and hosts; however, little is known about their biology. These new genomes of cycloviruses are the first from silver-haired bats, adding to the broader knowledge of cyclovirus diversity. With continuing studies, it is likely that additional viruses of the family Circoviridae will be identified in Arizona bat populations.

Evolutionary causes and consequences of ungulate migration.

Ungulate migrations are crucial for maintaining abundant populations and functional ecosystems. However, little is known about how or why migratory behaviour evolved in ungulates. To investigate the evolutionary origins of ungulate migration, we employed phylogenetic path analysis using a comprehensive species-level phylogeny of mammals. We found that 95 of 207 extant ungulate species are at least partially migratory, with migratory behaviour originating independently in 17 lineages. The evolution of migratory behaviour is associated with reliance on grass forage and living at higher latitudes wherein seasonal resource waves are most prevalent. Indeed, originations coincide with mid-Miocene cooling and the subsequent rise of C4 grasslands. Also, evolving migratory behaviour supported the evolution of larger bodies, allowing ungulates to exploit new ecological space. Reconstructions of migratory behaviour further revealed that seven of ten recently extinct species were probably migratory, suggesting that contemporary migrations are important models for understanding the ecology of the past.

A global ecological signal of extinction risk in terrestrial vertebrates.

To determine the distribution and causes of extinction threat across functional groups of terrestrial vertebrates, we assembled an ecological trait data set for 18,016 species of terrestrial vertebrates and utilized phylogenetic comparative methods to test which categories of habitat association, mode of locomotion, and feeding mode best predicted extinction risk. We also examined the individual categories of the International Union for Conservation of Nature Red List extinction drivers (e.g., agriculture and logging) threatening each species and determined the greatest threats for each of the four terrestrial vertebrate groups. We then quantified the sum of extinction drivers threatening each species to provide a multistressor perspective on threat. Cave dwelling amphibians (p < 0.01), arboreal quadrupedal mammals (all of which are primates) (p < 0.01), aerial and scavenging birds (p < 0.01), and pedal (i.e., walking) squamates (p < 0.01) were all disproportionately threatened with extinction in comparison with the other assessed ecological traits. Across all threatened vertebrate species in the study, the most common risk factors were agriculture, threatening 4491 species, followed by logging, threatening 3187 species, and then invasive species and disease, threatening 2053 species. Species at higher risk of extinction were simultaneously at risk from a greater number of threat types. If left unabated, the disproportionate loss of species with certain functional traits and increasing anthropogenic pressures are likely to disrupt ecosystem functions globally. A shift in focus from species- to trait-centric conservation practices will allow for protection of at-risk functional diversity from regional to global scales.

Una Señal Ecológica Mundial del Riesgo de Extinción de los Vertebrados Terrestres Resumen Construimos un conjunto de datos de atributos ecológicos de 18,016 especies de vertebrados terrestres y utilizamos métodos de comparación filogenética para analizar cuáles categorías de asociación de hábitat, modo de locomoción y modo de alimentación predicen de mejor manera el riesgo de extinción. Lo anterior lo hicimos para determinar la distribución y las causas de las amenazas de extinción a lo largo de los grupos funcionales de vertebrados terrestres. También examinamos las categorías individuales de los factores de extinción (p. ej.: agricultura, tala de árboles) de la Lista Roja de la Unión Internacional para la Conservación de la Naturaleza que amenazan a cada especie y determinamos las principales amenazas para cada uno de los cuatro grupos de vertebrados terrestres. Después cuantificamos la suma de los factores de extinción que amenazan a cada especie para proporcionar una perspectiva de estresores múltiples sobre la amenaza. Los anfibios cavernícolas (p < 0.01), mamíferos arbóreos cuadrúpedos (todos son primates) (p < 0.01), aves aéreas y carroñeras (p < 0.01) y los escamados caminantes (p < 0.01) tuvieron una amenaza de extinción desproporcionada en comparación con los otros atributos ecológicos analizados. En todas las especies de vertebrados que estudiamos, los factores de riesgo más comunes fueron la agricultura, que amenaza a 4,491 especies, y la deforestación, que amenaza a 3,187 especies; le siguen las especies invasoras y las enfermedades, que juntas amenazan a 2,053 especies. Las especies con el mayor riesgo de extinción también se encontraban simultáneamente en riesgo por un mayor número de tipos de amenazas. Si esto se mantiene constante, la pérdida desproporcionada de especies con ciertos atributos funcionales y la creciente presión antropogénica probablemente alteren las funciones ecosistémicas a nivel mundial. Un cambio en el enfoque de las prácticas de conservación, de estar centradas en la especie a estar centradas en los atributos, permitirá la protección de la diversidad funcional en riesgo desde la escala regional hasta la global.

Liberating host-virus knowledge from biological dark data.

Connecting basic data about bats and other potential hosts of SARS-CoV-2 with their ecological context is crucial to the understanding of the emergence and spread of the virus. However, when lockdowns in many countries started in March, 2020, the world's bat experts were locked out of their research laboratories, which in turn impeded access to large volumes of offline ecological and taxonomic data. Pandemic lockdowns have brought to attention the long-standing problem of so-called biological dark data: data that are published, but disconnected from digital knowledge resources and thus unavailable for high-throughput analysis. Knowledge of host-to-virus ecological interactions will be biased until this challenge is addressed. In this Viewpoint, we outline two viable solutions: first, in the short term, to interconnect published data about host organisms, viruses, and other pathogens; and second, to shift the publishing framework beyond unstructured text (the so-called PDF prison) to labelled networks of digital knowledge. As the indexing system for biodiversity data, biological taxonomy is foundational to both solutions. Building digitally connected knowledge graphs of host-pathogen interactions will establish the agility needed to quickly identify reservoir hosts of novel zoonoses, allow for more robust predictions of emergence, and thereby strengthen human and planetary health systems.

Evolutionary legacies in contemporary tetrapod imperilment.

The Tree of Life will be irrevocably reshaped as anthropogenic extinctions continue to unfold. Theory suggests that lineage evolutionary dynamics, such as age since origination, historical extinction filters and speciation rates, have influenced ancient extinction patterns - but whether these factors also contribute to modern extinction risk is largely unknown. We examine evolutionary legacies in contemporary extinction risk for over 4000 genera, representing ~30,000 species, from the major tetrapod groups: amphibians, birds, turtles and crocodiles, squamate reptiles and mammals. We find consistent support for the hypothesis that extinction risk is elevated in lineages with higher recent speciation rates. We subsequently test, and find modest support for, a primary mechanism driving this pattern: that rapidly diversifying clades predominantly comprise range-restricted, and extinction-prone, species. These evolutionary patterns in current imperilment may have important consequences for how we manage the erosion of biological diversity across the Tree of Life.

Molecules and fossils tell distinct yet complementary stories of mammal diversification.

Reconstructing the tempo at which biodiversity arose is a fundamental goal of evolutionary biologists, yet the relative merits of evolutionary-rate estimates are debated based on whether they are derived from the fossil record or time-calibrated phylogenies (timetrees) of living species. Extinct lineages unsampled in timetrees are known to "pull" speciation rates downward, but the temporal scale at which this bias matters is unclear. To investigate this problem, we compare mammalian diversification-rate signatures in a credible set of molecular timetrees (n = 5,911 species, ∼70% from DNA) to those in fossil genus durations (n = 5,320). We use fossil extinction rates to correct or "push" the timetree-based (pulled) speciation-rate estimates, finding a surge of speciation during the Paleocene (∼66-56 million years ago, Ma) between the Cretaceous-Paleogene (K-Pg) boundary and the Paleocene-Eocene Thermal Maximum (PETM). However, about two-thirds of the K-Pg-to-PETM originating taxa did not leave modern descendants, indicating that this rate signature is likely undetectable from extant lineages alone. For groups without substantial fossil records, thankfully all is not lost. Pushed and pulled speciation rates converge starting ∼10 Ma and are equal at the present day when recent evolutionary processes can be estimated without bias using species-specific "tip" rates of speciation. Clade-wide moments of tip rates also enable enriched inference, as the skewness of tip rates is shown to approximate a clade's extent of past diversification-rate shifts. Molecular timetrees need fossil-correction to address deep-time questions, but they are sufficient for shallower time questions where extinctions are fewer.

Holistic understanding of contemporary ecosystems requires integration of data on domesticated, captive and cultivated organisms.

Domestic and captive animals and cultivated plants should be recognised as integral components in contemporary ecosystems. They interact with wild organisms through such mechanisms as hybridization, predation, herbivory, competition and disease transmission and, in many cases, define ecosystem properties. Nevertheless, it is widespread practice for data on domestic, captive and cultivated organisms to be excluded from biodiversity repositories, such as natural history collections. Furthermore, there is a lack of integration of data collected about biodiversity in disciplines, such as agriculture, veterinary science, epidemiology and invasion science. Discipline-specific data are often intentionally excluded from integrative databases in order to maintain the "purity" of data on natural processes. Rather than being beneficial, we argue that this practise of data exclusivity greatly limits the utility of discipline-specific data for applications ranging from agricultural pest management to invasion biology, infectious disease prevention and community ecology. This problem can be resolved by data providers using standards to indicate whether the observed organism is of wild or domestic origin and by integrating their data with other biodiversity data (e.g. in the Global Biodiversity Information Facility). Doing so will enable efforts to integrate the full panorama of biodiversity knowledge across related disciplines to tackle pressing societal questions.

Where the wild things were: intrinsic and extrinsic extinction predictors in the world's most depleted mammal fauna.

Preventing extinctions requires understanding macroecological patterns of vulnerability or persistence. However, correlates of risk can be nonlinear, within-species risk varies geographically, and current-day threats cannot reveal drivers of past losses. We investigated factors that regulated survival or extinction in Caribbean mammals, which have experienced the globally highest level of human-caused postglacial mammalian extinctions, and included all extinct and extant Holocene island populations of non-volant species (219 survivals or extinctions across 118 islands). Extinction selectivity shows a statistically detectable and complex body mass effect, with survival probability decreasing for both mass extremes, indicating that intermediate-sized species have been more resilient. A strong interaction between mass and age of first human arrival provides quantitative evidence of larger mammals going extinct on the earliest islands colonized, revealing an extinction filter caused by past human activities. Survival probability increases on islands with lower mean elevation (mostly small cays acting as offshore refugia) and decreases with more frequent hurricanes, highlighting the risk of extreme weather events and rising sea levels to surviving species on low-lying cays. These findings demonstrate the interplay between intrinsic biology, regional ecology and specific local threats, providing insights for understanding drivers of biodiversity loss across island systems and fragmented habitats worldwide.

Genomic insights into the host specific adaptation of the Pneumocystis genus.

Pneumocystis jirovecii, the fungal agent of human Pneumocystis pneumonia, is closely related to macaque Pneumocystis. Little is known about other Pneumocystis species in distantly related mammals, none of which are capable of establishing infection in humans. The molecular basis of host specificity in Pneumocystis remains unknown as experiments are limited due to an inability to culture any species in vitro. To explore Pneumocystis evolutionary adaptations, we have sequenced the genomes of species infecting macaques, rabbits, dogs and rats and compared them to available genomes of species infecting humans, mice and rats. Complete whole genome sequence data enables analysis and robust phylogeny, identification of important genetic features of the host adaptation, and estimation of speciation timing relative to the rise of their mammalian hosts. Our data reveals insights into the evolution of P. jirovecii, the sole member of the genus able to infect humans.

Wanted: Standards for FAIR taxonomic concept representations and relationships.

Making the most of biodiversity data requires linking observations of biological species from multiple sources both efficiently and accurately (Bisby 2000, Franz et al. 2016). Aggregating occurrence records using taxonomic names and synonyms is computationally efficient but known to experience significant limitations on accuracy when the assumption of one-to-one relationships between names and biological entities breaks down (Remsen 2016, Franz and Sterner 2018). Taxonomic treatments and checklists provide authoritative information about the correct usage of names for species, including operational representations of the meanings of those names in the form of range maps, reference genetic sequences, or diagnostic traits. They increasingly provide taxonomic intelligence in the form of precise description of the semantic relationships between different published names in the literature. Making this authoritative information Findable, Accessible, Interoperable, and Reusable (FAIR; Wilkinson et al. 2016) would be a transformative advance for biodiversity data sharing and help drive adoption and novel extensions of existing standards such as the Taxonomic Concept Schema and the OpenBiodiv Ontology (Kennedy et al. 2006, Senderov et al. 2018). We call for the greater, global Biodiversity Information Standards (TDWG) and taxonomy community to commit to extending and expanding on how FAIR applies to biodiversity data and include practical targets and criteria for the publication and digitization of taxonomic concept representations and alignments in taxonomic treatments, checklists, and backbones.

Inferring the mammal tree: Species-level sets of phylogenies for questions in ecology, evolution, and conservation.

Big, time-scaled phylogenies are fundamental to connecting evolutionary processes to modern biodiversity patterns. Yet inferring reliable phylogenetic trees for thousands of species involves numerous trade-offs that have limited their utility to comparative biologists. To establish a robust evolutionary timescale for all approximately 6,000 living species of mammals, we developed credible sets of trees that capture root-to-tip uncertainty in topology and divergence times. Our "backbone-and-patch" approach to tree building applies a newly assembled 31-gene supermatrix to two levels of Bayesian inference: (1) backbone relationships and ages among major lineages, using fossil node or tip dating, and (2) species-level "patch" phylogenies with nonoverlapping in-groups that each correspond to one representative lineage in the backbone. Species unsampled for DNA are either excluded ("DNA-only" trees) or imputed within taxonomic constraints using branch lengths drawn from local birth-death models ("completed" trees). Joining time-scaled patches to backbones results in species-level trees of extant Mammalia with all branches estimated under the same modeling framework, thereby facilitating rate comparisons among lineages as disparate as marsupials and placentals. We compare our phylogenetic trees to previous estimates of mammal-wide phylogeny and divergence times, finding that (1) node ages are broadly concordant among studies, and (2) recent (tip-level) rates of speciation are estimated more accurately in our study than in previous "supertree" approaches, in which unresolved nodes led to branch-length artifacts. Credible sets of mammalian phylogenetic history are now available for download at http://vertlife.org/phylosubsets, enabling investigations of long-standing questions in comparative biology.