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Emerling, C. A.

Publications and source records attributed to Emerling, C. A..

5 recordsLinked to original sources

Pseudogenes document protracted parallel regression of oral anatomy in myrmecophagous mammals

Adaptation to ant and/or termite consumption (myrmecophagy) in mammals constitutes a textbook example of convergent evolution, being independently derived in several mammalian lineages. Myrmecophagous species are characterized by striking convergent morphological adaptations such as skull elongation, enlargement of salivary glands, and long claws to dig into ant and termite nests. These evolutionary modifications also include anatomical regression, such as dental simplification or loss, reduction of masticatory muscles, and possessing a reduced set of taste buds. To gain insights into the molecular changes underlying the regression of these morpho-anatomical traits, we investigated the functionality of candidate genes related to dentition, gustation, and mastication in nine convergent myrmecophagous mammalian lineages. We examined these genes in a comparative phylogenetic context, paired with molecular evolutionary analyses, to estimate the relative timing of loss of gene function over the evolutionary history of each convergent lineage. We found that gustatory reduction and pseudogenization of masticatory myosin often were associated with the regression of dental genes. Evidence of pseudogenization events linked to oral anatomy dates to as early as the Cretaceous/Paleogene boundary, and is an ongoing process including examples of incipient gene inactivations. Whereas we found evidence for gene inactivations across all three functional categories occurring during distinct temporal intervals, there was variation in the sets of genes lost and the relative timing of inactivation events. The combined evidence suggests that the convergent evolution of myrmecophagy has occurred as a protracted process with distinct phases of anatomical evolution, over timescales as long as 60 Myr.

evolutionary biology↗

Genomic data suggest parallel dental vestigialization within the xenarthran radiation

AO_SCPLOWBSTRACTC_SCPLOWThe recent influx of genomic data has provided greater insights into the molecular basis for regressive evolution, or vestigialization, through gene loss and pseudogenization. As such, the analysis of gene degradation patterns has the potential to provide insights into the evolutionary history of regressed anatomical traits. We specifically applied these principles to the xenarthran radiation (anteaters, sloths, armadillos), which is characterized by taxa with a gradation in regressed dental phenotypes. Whether the pattern among extant xenarthrans is due to an ancient and gradual decay of dental morphology or occurred repeatedly in parallel is unknown. We tested these competing hypotheses by examining 11 core dental genes in most living species of Xenarthra, characterizing shared inactivating mutations and patterns of relaxed selection during their radiation. Here we report evidence of independent and distinct events of dental gene loss in the major xenarthran subclades. First, we found strong evidence of complete enamel loss in the common ancestor of sloths and anteaters, suggested by the inactivation of five enamel-associated genes (AMELX, AMTN, MMP20, ENAM, ACP4). Next, whereas dental regression appears to have halted in sloths, presumably a critical event that ultimately permitted adaptation to an herbivorous lifestyle, anteaters continued losing genes on the path towards complete tooth loss. Echoes of this event are recorded in the genomes of all living anteaters, being marked by a 2-bp deletion in a gene critical for dentinogenesis (DSPP) and a putative shared 1-bp insertion in a gene linked to tooth retention (ODAPH). By contrast, in the two major armadillo clades, genes pertaining to the dento-gingival junction and amelogenesis appear to have been independently inactivated prior to losing all or some enamel. These genomic data provide evidence for multiple pathways and rates of anatomical regression, and underscore the utility of using pseudogenes to reconstruct evolutionary history when fossils are sparse.

evolutionary biology↗

Comparative transcriptomics reveals divergent paths of chitinase evolution underlying dietary convergence in ant-eating mammals

Ant-eating mammals represent a textbook example of convergent evolution. Among them, anteaters and pangolins exhibit the most extreme convergent phenotypes with complete tooth loss, elongated skulls, protruding tongues, hypertrophied salivary glands producing large amounts of saliva, and powerful claws for ripping open ant and termite nests. However, comparative genomic analyses have shown that anteaters and pangolins differ in their chitinase acidic gene (CHIA) repertoires, which potentially degrade the chitinous exoskeletons of ingested ants and termites. While the southern tamandua (Tamandua tetradactyla) harbors four functional CHIA paralogs (CHIA1-4), Asian pangolins (Manis spp.) have only one functional paralog (CHIA5). Here, we performed a comparative transcriptomic analysis of salivary glands in 33 placental species, including 16 novel transcriptomes from ant-eating species and close relatives. Our results suggest that salivary glands play an important role in adaptation to an insect-based diet, as expression of different CHIA paralogs is observed in insectivorous species. Furthermore, convergently-evolved pangolins and anteaters express different chitinases in their digestive tracts. In the Malayan pangolin, CHIA5 is overexpressed in all major digestive organs, whereas in the southern tamandua, all four functional paralogs are expressed, at very high levels for CHIA1 and CHIA2 in the pancreas, and for CHIA3 and CHIA4 in the salivary glands, stomach, liver, and pancreas. Overall, our results demonstrate that divergent molecular mechanisms within the chitinase acidic gene family underlie convergent adaptation to the ant-eating diet in pangolins and anteaters. This study highlights the role of historical contingency and molecular tinkering of the chitin-digestive enzyme toolkit in this classic example of convergent evolution.

evolutionary biology↗

Independent pseudogenization of CYP2J19 in penguins, owls and kiwis implicates gene in red carotenoid synthesis

Carotenoids have important roles in bird behavior, including pigmentation for sexual signaling and improving color vision via retinal oil droplets. Yellow carotenoids are diet-derived, but red carotenoids (ketocarotenoids) are typically synthesized from yellow precursors via a carotenoid ketolase. Recent research on passerines has provided evidence that a cytochrome p450 enzyme, CYP2J19, is responsible for this reaction, though it is unclear if this function is phylogenetically restricted. Here I provide evidence that CYP2J19 is the carotenoid ketolase common to Aves using the genomes of 65 birds and the retinal transcriptomes of 15 avian taxa. CYP2J19 is functionally intact and robustly transcribed in all taxa except for several species adapted to foraging in dim light conditions. Two penguins, an owl and a kiwi show evidence of genetic lesions and relaxed selection in their genomic copy of CYP2J19, and six owls show evidence of marked reduction in CYP2J19 retinal transcription compared to nine diurnal avian taxa. Notably, none of these taxa are known to use red carotenoids for sexual signaling and several species of owls and penguins represent the only birds known to completely lack red retinal oil droplets. The remaining avian taxa belong to groups known to possess red oil droplets, known or expected to deposit red carotenoids in skin and/or plumage, and/or frequently forage in bright light. The loss and reduced expression of CYP2J19 is likely an adaptation to maximize retinal sensitivity, given that oil droplets reduce the amount of light available to the retina.

evolutionary biology↗

Genomic regression of claw keratin, taste receptor and light-associated genes inform biology and evolutionary origins of snakes

Regressive evolution of anatomical traits corresponds with the regression of genomic loci underlying such characters. As such, studying patterns of gene loss can be instrumental in addressing questions of gene function, resolving conflicting results from anatomical studies, and understanding the evolutionary history of clades. The origin of snakes coincided with the regression of a number of anatomical traits, including limbs, taste buds and the visual system. By studying the genomes of snakes, I was able to test three hypotheses associated with the regression of these features. The first concerns two keratins that are putatively specific to claws. Both genes that encode these keratins were pseudogenized/deleted in snake genomes, providing additional evidence of claw- specificity. The second hypothesis is whether snakes lack taste buds, an issue complicated by unequivocal, conflicting results in the literature. I found evidence that different snakes have lost one or more taste receptors, but all snakes examined retained at least some capacity for taste. The final hypothesis I addressed is that the earliest snakes were adapted to a dim light niche. I found evidence of deleted and pseudogenized genes with light- associated functions in snakes, demonstrating a pattern of gene loss similar to other historically nocturnal clades. Together these data also provide some bearing on the ecological origins of snakes, including molecular dating estimates that suggest dim light adaptation preceded the loss of limbs.

evolutionary biology↗