Immigration dynamics of tropical and subtropical Southeast Asian limestone karst floras

Ex situ origins and dispersal of taxa have played important roles in the assembly of island-like biodiversity hotspots. Insular limestone karsts in Southeast Asia are hotspots of biodiversity and endemism, but the immigration processes of their unique floras are still poorly known. Here, we used Gesneriaceae as a proxy to investigate the immigration dynamics of tropical and subtropical Southeast Asian karst floras. We present the most comprehensive phylogenetic analysis of the Old World gesneriads to date based on twelve loci. By estimating divergence times and reconstructing ancestral states (habitat, soil type and range), we found that immigration into subtropical Southeast Asian karst floras first occurred in the Early Miocene, with two peaks in the Early–Middle Miocene and the Pliocene–Early Pleistocene, whereas immigration into tropical Southeast Asian karsts initiated in the Late Eocene, with two peaks in the Late Oligocene and the Late Miocene. We also discover that Southeast Asian karst biodiversity comprises immigrant pre-adapted lineages and descendants from local acid soil ancestors, although niche shift from acid soil to karst in tropical Southeast Asian islands was lacking. This study advances our understanding of the historical assembly of Southeast Asian karst floras.

Life History and the Transitions to Eusociality in the Hymenoptera

Although indirect selection through relatives (kin selection) can explain the evolution of effectively sterile offspring that act as helpers at the nest (eusociality) in the ants, bees, and stinging wasps (aculeate Hymenoptera), the genetic, ecological, and life history conditions that favor transitions to eusociality are poorly understood. In this study, ancestral state reconstruction on recently published phylogenies was used to identify the independent transitions to eusociality in each of the taxonomic families that exhibit eusociality. Semisociality, in which a single nest co-foundress monopolizes reproduction, often precedes eusociality outside the vespid wasps. Such a route to eusociality, which is consistent with groups consisting of a mother and her daughters (subsocial) at some stage and ancestral monogamy, is favored by the haplodiploid genetic sex determination of the Hymenoptera (diploid females and haploid males) and thus may explain why eusociality is common in the Hymenoptera. Ancestral states were also reconstructed for life history characters that have been implicated in the origins of eusociality. A loss of larval diapause during unfavorable seasons or conditions precedes, or coincides with, all but one transition to eusociality. This pattern is confirmed using phylogenetic tests of associations between state transition rates for sweat bees and apid bees. A loss of larval diapause may simply reflect the subsocial route to eusociality since subsociality is defined as females interacting with their adult daughters. A loss of larval diapause and a gain of subsociality may be associated with an extended breeding season that permits the production of at least two broods, which is necessary for helpers to evolve. Adult diapause may also lower the selective barrier to a first-brood daughter becoming a helper. Obligate eusociality meets the definition of a major evolutionary transition, and such transitions have occurred five times in the Hymenoptera.

Evolutionary history of sexual differentiation mechanism in insects

Gain of alternative splicing gives rise to functional diversity in proteins and underlies the complexity and diversity of biological aspects. However, it is still not fully understood how alternatively spliced genes develop the functional novelty. To this end, we infer the evolutionary history of the doublesex gene, the key transcriptional factor in the sexual differentiation of arthropods. doublesex is controlled by sex-specific splicing and promotes both male and female differentiation in some holometabolan insects. In contrast, doublesex promotes only male differentiation in some hemimetabolan insects. Here, we investigate ancestral states of doublesex using Thermobia domestica belonging to Zygentoma, the sister group of winged insects. We find that doublesex of T. domestica expresses sex-specific isoforms but is only necessary for male differentiation of sexual morphology. This result ensures the hypothesis that doublesex was initially only used to promote male differentiation during insect evolution. However, T. domestica doublesex has a short female-specific region and upregulates the expression of vitellogenin homologs in females, suggesting that doublesex may have already controlled some aspects of feminization in the common ancestor of winged insects. Reconstruction of the ancestral sequence and prediction of the protein structure show that the female-specific isoform of doublesex has a long C-terminal disordered region in holometabolan insects, but not in non-holometabolan species. We propose that doublesex acquired a female-specific isoform and then underwent a change in the protein motif structure, which became essential for female differentiation in sexual dimorphisms.

Morphological and Phylogenetic Reevaluation of the Genera Mycobonia and Pseudofavolus (Polyporaceae)

Mycobonia and Pseudofavolus (Polyporales, Basidiomycota) are polyporoid genera with tropical and subtropical distribution. Both genera are morphologically similar in presenting flabelliform to conchate subsessile basidiomata, with a dimitic hyphal system, consisting of clamped generative hyphae and skeleto-binding hyphae that produce large basidiospores with smooth, thin walls. However, while Pseudofavolus species present a poroid hymenophore, in Mycobonia it is stereoid with hyphal pegs that resemble thin teeth. Mycobonia and Pseudofavolus have a controversial taxonomy, and the phylogenetic relationships between their species have yet to be assessed. For this reason, we performed molecular phylogenetic analyses on specimens of Mycobonia and Pseudofavolus from both the Neotropics and Asia, using internal transcribed spacers (ITS), the large subunit of nuclear rDNA (nc LSU rDNA), and also the genes encoding the second largest subunit of RNA polymerase II (RPB2). Furthermore, in order to develop an evolutionary analysis of the hymenophore configuration, we performed stochastic character mapping of ancestral states for the hymenophore type presented in Polyporus s.l. Our study revealed that Pseudofavolus is an artificial group and its species actually nest in a clade within Mycobonia. Therefore, in order to establish a monophyletic group, based upon priority of publication, we re-circunscribed Mycobonia to encompass both stereoid and poroid hymenophore species. Two new combinations are presented from the Neotropics: Mycobonia cucullata and M. miquelii. A new species from tropical Asia, M. yuchengii, is also described. We presente a summary of stochastic mapping of ancestral states estimates of hymenophore type in Polyporus s.l. The ancestral state for Mycobonia clade is estimated to have angular pores.

Recombination and lineage-specific mutations linked to the emergence of SARS-CoV-2

Background The emergence of SARS-CoV-2 underscores the need to better understand the evolutionary processes that drive the emergence and adaptation of zoonotic viruses in humans. In the betacoronavirus genus, which also includes SARS-CoV and MERS-CoV, recombination frequently encompasses the receptor binding domain (RBD) of the Spike protein, which is responsible for viral binding to host cell receptors. In this work, we reconstruct the evolutionary events that have accompanied the emergence of SARS-CoV-2, with a special emphasis on the RBD and its adaptation for binding to its receptor, human ACE2. Methods By means of phylogenetic and recombination analyses, we found evidence of a recombination event in the RBD involving ancestral linages to both SARS-CoV and SARS-CoV-2. We then assessed the effect of this recombination at protein level by reconstructing the RBD of the closest ancestors to SARS-CoV-2, SARS-CoV, and other Sarbecoviruses, including the most recent common ancestor of the recombining clade. The resulting information was used to measure and compare, in silico, their ACE2-binding affinities using the physics-based trRosetta algorithm. Results We show that, through an ancestral recombination event, SARS-CoV and SARS-CoV-2 share an RBD sequence that includes two insertions (positions 432-436 and 460-472), as well as the variants 427N and 436Y. Both 427N and 436Y belong to a helix that interacts directly with the human ACE2 (hACE2) receptor. Reconstruction of ancestral states, combined with protein-binding affinity analyses, suggests that the recombination event involving ancestral strains of SARS-CoV and SARS-CoV-2 led to an increased affinity for hACE2 binding and that alleles 427N and 436Y significantly enhanced affinity as well. Conclusions We report an ancestral recombination event affecting the RBD of both SARS-CoV and SARS-CoV-2 that was associated with an increased binding affinity to hACE2. Structural modeling indicates that ancestors of SARS-CoV-2 may have acquired the ability to infect humans decades ago. The binding affinity with the human receptor would have been subsequently boosted in SARS-CoV and SARS-CoV-2 through further mutations in RBD.

Reconstructing unobserved cellular states from paired single-cell lineage tracing and transcriptomics data

Novel experimental assays now simultaneously measure lineage relationships and transcriptomic states from single cells, thanks to CRISPR/Cas9-based genome engineering. These multimodal measurements allow researchers not only to build comprehensive phylogenetic models relating all cells but also infer transcriptomic determinants of consequential subclonal behavior. The gene expression data, however, is limited to cells that are currently present ("leaves" of the phylogeny). As a consequence, researchers cannot form hypotheses about unobserved, or "ancestral", states that gave rise to the observed population. To address this, we introduce TreeVAE: a probabilistic framework for estimating ancestral transcriptional states. TreeVAE uses a variational autoencoder (VAE) to model the observed transcriptomic data while accounting for the phylogenetic relationships between cells. Using simulations, we demonstrate that TreeVAE outperforms benchmarks in reconstructing ancestral states on several metrics. TreeVAE also provides a measure of uncertainty, which we demonstrate to correlate well with its prediction accuracy. This estimate therefore potentially provides a data-driven way to estimate how far back in the ancestor chain predictions could be made. Finally, using real data from lung cancer metastasis, we show that accounting for phylogenetic relationship between cells improves goodness of fit. Together, TreeVAE provides a principled framework for reconstructing unobserved cellular states from single cell lineage tracing data.

Evolutionary history of mental glands in turtles reveals a single origin in an aquatic ancestor and recurrent losses independent of macrohabitat

Despite the relevance of chemical communication in vertebrates, comparative examinations of macroevolutionary trends in chemical signaling systems are scarce. Many turtle and tortoise species are reliant on chemical signals to communicate in aquatic and terrestrial macrohabitats, and many of these species possess specialized integumentary organs, termed mental glands (MGs), involved in the production of chemosignals. We inferred the evolutionary history of MGs and tested the impact of macrohabitat on their evolution. Inference of ancestral states along a time-calibrated phylogeny revealed a single origin in the ancestor of the subclade Testudinoidea. Thus, MGs represent homologous structures in all descending lineages. We also inferred multiple independent losses of MGs in both terrestrial and aquatic clades. Although MGs first appeared in an aquatic turtle (the testudinoid ancestor), macrohabitat seems to have had little effect on MG presence or absence in descendants. Instead, we find clade-specific evolutionary trends, with some clades showing increased gland size and morphological complexity, whereas others exhibiting reduction or MG loss. In sister clades inhabiting similar ecological niches, contrasting patterns (loss vs. maintenance) may occur. We conclude that the multiple losses of MGs in turtle clades have not been influenced by macrohabitat and that other factors have affected MG evolution.

Refining Convergent Rate Analysis with Topology in Mammalian Longevity and Marine Transitions

The quest to map the genetic foundations of phenotypes has been empowered by the modern diversity, quality, and availability of genomic resources. Despite these expanding resources, the abundance of variation within lineages makes the association of genetic change to specific phenotypes improbable. Drawing such connections requires an a priori means of isolating the associated changes from background genomic variation. Evolution may provide these means via convergence; i.e., the shared variation that may result from replicate evolutionary experiments across independent trait occurrences. To leverage these opportunities, we developed TRACCER: Topologically Ranked Analysis of Convergence via Comparative Evolutionary Rates. As compared to current methods, this software empowers rate convergence analysis by factoring in topological relationships, because variation between phylogenetically proximate trait changes is more likely to be facilitating the trait. Pairwise comparisons are performed not with singular branches, but in reference to their most recent common ancestors. This ensures that comparisons represent identical genetic contexts and timeframes while obviating the problematic requirement of assigning ancestral states. We applied TRACCER to two case studies: marine mammal transitions, an unambiguous trait which has independently evolved three times, as well as the evolution of mammalian longevity, a less delineated trait but with more instances to compare. TRACCER, by factoring in topology, identifies highly significant, convergent genetic signals in these test cases, with important incongruities and statistical resolution when compared to existing convergence approaches. These improvements in sensitivity and specificity generate refined targets for downstream analysis of convergent evolution and identification of genotype-phenotype relationships.

Loss of Active Neurogenesis in the Adult Shark Retina

Neurogenesis is the process by which progenitor cells generate new neurons. As development progresses neurogenesis becomes restricted to discrete neurogenic niches, where it persists during postnatal life. The retina of teleost fishes is thought to proliferate and produce new cells throughout life. Whether this capacity may be an ancestral characteristic of gnathostome vertebrates is completely unknown. Cartilaginous fishes occupy a key phylogenetic position to infer ancestral states fixed prior to the gnathostome radiation. Previous work from our group revealed that the juvenile retina of the catshark Scyliorhinus canicula, a cartilaginous fish, shows active proliferation and neurogenesis. Here, we compared the morphology and proliferative status of the retina in catshark juveniles and adults. Histological and immunohistochemical analyses revealed an important reduction in the size of the peripheral retina (where progenitor cells are mainly located), a decrease in the thickness of the inner nuclear layer (INL), an increase in the thickness of the inner plexiform layer and a decrease in the cell density in the INL and in the ganglion cell layer in adults. Contrary to what has been reported in teleost fish, mitotic activity in the catshark retina was virtually absent after sexual maturation. Based on these results, we carried out RNA-Sequencing (RNA-Seq) analyses comparing the retinal transcriptome of juveniles and adults, which revealed a statistically significant decrease in the expression of many genes involved in cell proliferation and neurogenesis in adult catsharks. Our RNA-Seq data provides an excellent resource to identify new signaling pathways controlling neurogenesis in the vertebrate retina.

Investigation of ancestral alleles in the Bovinae subfamily

Background In evolutionary theory, divergence and speciation can arise from long periods of reproductive isolation, genetic mutation, selection and environmental adaptation. After divergence, alleles can either persist in their initial state (ancestral allele - AA), co-exist or be replaced by a mutated state (derived alleles -DA). In this study, we aligned whole genome sequences of individuals from the Bovinae subfamily to the cattle reference genome (ARS.UCD-1.2) for defining ancestral alleles necessary for selection signatures study. Results Accommodating independent divergent of each lineage from the initial ancestral state, AA were defined based on fixed alleles on at least two groups of yak, bison and gayal-gaur-banteng resulting in ~ 32.4 million variants. Using non-overlapping scanning windows of 10 Kb, we counted the AA observed within taurine and zebu cattle. We focused on the extreme points, regions with top 0. 1% (high count) and regions without any occurrence of AA (null count). High count regions preserved gene functions from ancestral states that are still beneficial in the current condition, while null counts regions were linked to mutated ones. For both cattle, high count regions were associated with basal lipid metabolism, essential for survival of various environmental pressures. Mutated regions were associated to productive traits in taurine, i.e. higher metabolism, cell development and behaviors and in immune response domain for zebu. Conclusions Our findings suggest that retaining and losing AA in some regions are varied and made it species-specific with possibility of overlapping as it depends on the selective pressure they had to experience.