Laurel R. Yohe

Trpc2 pseudogenization dynamics in bats reveal ancestral vomeronasal signaling, then pervasive loss.

Comparative methods are often used to infer loss or gain of complex phenotypes, but few studies take advantage of genes tightly linked with complex traits to test for shifts in the strength of selection. In mammals, vomerolfaction detects chemical cues mediating many social and reproductive behaviors and is highly conserved, but all bats exhibit degraded vomeronasal structures with the exception of two families (Phyllostomidae and Miniopteridae). These families either regained vomerolfaction after ancestral loss, or there were many independent losses after diversification from an ancestor with functional vomerolfaction. In this study, we use the Transient receptor potential cation channel 2 (Trpc2) as a molecular marker for testing the evolutionary mechanisms of loss and gain of the mammalian vomeronasal system. We sequenced Trpc2 exon 2 in over 100 bat species across 17 of 20 chiropteran families. Most families showed independent pseudogenizing mutations in Trpc2, but the reading frame was highly conserved in phyllostomids and miniopterids. Phylogeny‐based simulations suggest loss of function occurred after bat families diverged, and purifying selection in two families has persisted since bats shared a common ancestor. As most bats still display pheromone‐mediated behavior, they might detect pheromones through the main olfactory system without using the Trpc2 signaling mechanism.

Evidence for multifactorial processes underlying phenotypic variation in bat visual opsins

Studies of opsin genes offer insights into the evolutionary history and molecular basis of vertebrate color vision, but most assume intact open reading frames equate to functional phenotypes. Despite known variation in opsin repertoires and associated visual phenotypes, the genetic basis of such patterns has not been examined at each step of the central dogma. By comparing sequences, gene expression, and protein localization across a hyperdiverse group of mammals, noctilionoid bats, we find evidence that independent losses of S-opsin arose through disruptions at different stages of protein synthesis, while maintenance relates to frugivory. Discordance between DNA, RNA, and protein reveals that the loss of short-wave sensitivity in some lineages resulted from transcriptional and post-transcriptional changes in addition to degradation of open reading frames. These mismatches imply that visual phenotypes cannot reliably be predicted from genotypes alone, and connect ecology to multiple mechanisms behind the loss of color in vertebrates.

Bayesian hierarchical models suggest oldest known plant-visiting bat was omnivorous

The earliest record of plant visiting in bats dates to the Middle Miocene of La Venta, the worlds most diverse tropical palaeocommunity. Palynephyllum antimaster is known from molars that indicate nectarivory. Skull length, an important indicator of key traits such as body size, bite force and trophic specialization, remains unknown. We developed Bayesian models to infer skull length based on dental measurements. These models account for variation within and between species, variation between clades, and phylogenetic error structure. Models relating skull length to trophic level for nectarivorous bats were then used to infer the diet of the fossil. The skull length estimate for Palynephyllum places it among the larger lonchophylline bats. The inferred diet suggests Palynephyllum fed on nectar and insects, similar to its living relatives. Omnivory has persisted since the mid-Miocene. This is the first study to corroborate with fossil data that highly specialized nectarivory in bats requires an omnivorous transition.

Protocols for the Molecular Evolutionary Analysis of Membrane Protein Gene Duplicates

Gene duplication is an important process in the evolution of gene content in eukaryotic genomes. Understanding when gene duplicates contribute new molecular functions to genomes through molecular adaptation is one important goal in comparative genomics. In large gene families, however, characterizing adaptation and neofunctionalization across species is challenging, as models have traditionally quantified the timing of duplications without considering underlying gene trees. This protocol combines multiple approaches to detect adaptation in protein duplicates at a phylogenetic scale. We include a description of models for gene tree-species tree reconciliation that enable different types of inference, as well as a practical guide to their use. Although simulation-based approaches successfully detect shifts in the rate of duplication/retention, the conflation between the duplication and retention processes, the distinct trajectories of duplicates under non-, sub-, and neofunctionalization, as well as dosage effects offer hitherto unexplored analytical avenues. We introduce mathematical descriptions of these probabilities and offer a road map to computational implementation whose starting point is parsimony reconciliation. Sequence evolution information based on the ratio of nonsynonymous to synonymous nucleotide substitution rates (dN/dS) can be combined with duplicate survival probabilities to better predict the emergence of new molecular functions in retained duplicates. Together, these methods enable characterization of potentially adaptive candidate duplicates whose neofunctionalization may contribute to phenotypic divergence across species.

Expressed vomeronasal type-1 receptors (V1rs) in bats uncover conserved mechanisms of social chemical signaling

In mammals, social and reproductive behaviors are mediated by chemical cues encoded by hyperdiverse families of receptors expressed in the vomeronasal organ. Between species, the number of intact receptors can vary by orders of magnitude. However, the evolutionary processes behind variation in receptor number, and also its link to fitness-related behaviors are not well understood. From vomeronasal transcriptomes, we discovered the first evidence of intact vomeronasal type-1 receptor (V1r) genes in bats, and we tested whether putatively functional bat receptors were orthologous to those of related taxa, or whether bats have evolved novel receptors. We found that V1rs in bats and show high levels of orthology to those of their relatives, as opposed to lineage-specific duplications, and receptors are under purifying selection. Despite widespread vomeronasal organ loss in bats, V1r copies have been retained for >65 million years. The highly conserved nature of bat V1rs challenges our current understanding of mammalian V1r function and suggest roles other than conspecific recognition or mating initiation in social behavior.

Vomeronasal and Olfactory Structures in Bats Revealed by DiceCT Clarify Genetic Evidence of Function

The degree to which molecular and morphological loss of function occurs synchronously during the vestigialization of traits is not well understood. The mammalian vomeronasal system, a sense critical for mediating many social and reproductive behaviors, is highly conserved across mammals. New World Leaf-nosed bats (Phyllostomidae) are under strong selection to maintain a functional vomeronasal system such that most phyllostomids possess a distinct vomeronasal organ and an intact TRPC2, a gene encoding a protein primarily involved in vomeronasal sensory neuron signal transduction. Recent genetic evidence, however, shows that TRPC2 is a pseudogene in some Caribbean nectarivorous phyllostomids. The loss-of-function mutations suggest the sensory neural tissue of the vomeronasal organ is absent in these species despite strong selection on this gene in its mainland relatives, but the anatomy was unknown in most Caribbean nectarivorous phyllostomids until this study. We used diffusible iodine-based contrast-enhanced computed tomography (diceCT) to test whether the vomeronasal and main olfactory anatomy of several phyllostomid species matched genetic evidence of function, providing insight into whether loss of a structure is linked to pseudogenization of a molecular component of the system. The vomeronasal organ is indeed rudimentary or absent in species with a disrupted TRPC2 gene. Caribbean nectar-feeders also exhibit derived olfactory turbinal morphology and a large olfactory recess that differs from closely related bats that have an intact vomeronasal organ, which may hint that the main olfactory system may compensate for loss. We emphasize non-invasive diceCT is capable of detecting the vomeronasal organ, providing a feasible approach for quantifying mammalian chemosensory anatomy across species.

Unveiling the impact of human influence on species distributions in Vietnam: a case study using babblers (Aves: Timaliidae)

As developing countries give priority to economic growth, the effects of development threaten natural habitats and species distributions. Over the course of two decades, Vietnam has rapidly developed, especially in the expansion of agricultural production. However, no study has quantitatively measured the effects of recent human impact on the effects of past species distributions in Vietnam. We use locality data collected from multiple natural history collections, including several in Vietnam, to infer past species distributions. We assess habitat availability of five common babbler species (Aves: Timaliidae) using distribution models with data prior to rapid development that followed political reform. Overlaying the Global Human Influence Index with predicted distributions highlights the human impact on these distributions. Three important patterns emerge: (1) human impact influences common Timaliidae distributions similarly, (2) widespread species distributions show higher fragmentation due to human influence compared to narrowly distributed species in Vietnam, and (3) less than 20% of distributions overlap with nationally declared protected areas. We emphasize that conservation efforts should not only prioritize individual species, but also focus efforts on a regional scale, and that the use of museum data can be highly informative in conservation analyses. There are current obstacles to enforcing conservation of Vietnams already fragmented habitats, but our results suggest there is still time to reevaluate conservation approaches.