Islands are natural laboratories for studying patterns and processes of evolution. Research on island endemic birds has revealed elevated speciation rates and rapid phenotypic evolution in several groups (e.g. white-eyes, Darwin’s finches). However, understanding the evolutionary processes behind these patterns requires an understanding of how genotypes map to novel phenotypes. To date, there are few high-quality reference genomes for species found on islands. Here, we sequence the genome of one of Ernst Mayr’s “great speciators,” the collared kingfisher (Todiramphus chloris collaris). Utilizing high molecular weight DNA and linked-read sequencing technology, we assembled a draft high-quality genome with highly contiguous scaffolds (scaffold N50 = 19 Mb). Based on universal single-copy orthologs, we estimated a gene space completeness of 96.6% for the draft genome assembly. The population demographic history analyses reveal a distinct pattern of contraction and expansion in population size throughout the Pleistocene. Comparative genomic analysis of gene family evolution revealed that species-specific and rapidly expanding gene families in the collared kingfisher (relative to other Coraciiformes) are mainly involved in the ErbB signaling pathway and focal adhesion. Todiramphus kingfishers are a species-rich group that has become a focus of speciation research. This draft genome will be a platform for future taxonomic, phylogeographic, and speciation research in the group. For example, target genes will enable testing of changes in sensory structures associated with changes in vision and taste genes across kingfishers.
Understanding the genetic basis of convergence at broad phylogenetic scales remains a key challenge in biology. Kingfishers (Aves: Alcedinidae) are a cosmopolitan avian radiation with diverse colors, diets, and feeding behaviors—including the archetypal plunge-dive into water. Given the sensory and locomotor challenges associated with air-water transitions, kingfishers offer a powerful opportunity to explore the effects of convergent behaviors on the evolution of genomes and phenotypes, as well as direct comparisons between continental and island lineages. Here, we use whole-genome sequencing of 30 diverse kingfisher species to identify the genomic signatures associated with convergent feeding behaviors. We show that species with smaller ranges (i.e., on islands) have experienced stronger demographic fluctuations than those on continents, and that these differences have influenced the dynamics of molecular evolution. Comparative genomic analyses reveal positive selection and genomic convergence in brain and dietary genes in plunge-divers. These findings enhance our understanding of the connections between genotype and phenotype in a diverse avian radiation.
more » « less- Award ID(s):
- 2112468
- PAR ID:
- 10470560
- Publisher / Repository:
- Nature Publishing Group
- Date Published:
- Journal Name:
- Communications Biology
- Volume:
- 6
- Issue:
- 1
- ISSN:
- 2399-3642
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
Abstract -
Abstract The paradox of the great speciators describes a contradictory biogeographic pattern exhibited by numerous avian lineages in Oceania. Specifically, these lineages display broad geographic distributions across the region, implying strong over-water dispersal capabilities; yet, they also display repeated genetic and phenotypic divergence—even between geographically proximate islands—implying poor inter-island dispersal capabilities. One group originally cited as evidence for this paradox is the dwarf kingfishers of the genus Ceyx. Here, using genomic sequencing and comprehensive geographic sampling of the monophyletic Ceyx radiation from northern Melanesia, we find repeated, deep genetic divergence and no evidence for gene flow between lineages found on geographically proximate islands, providing an exceptionally clear example of the paradox of the great speciators. A dated phylogenetic reconstruction suggests a significant burst of diversification occurred rapidly after reaching northern Melanesia, between 3.9 and 2.9 MYA. This pattern supports a shift in net diversification rate, concordant with the expectations of the “colonization cycle” hypothesis, which implies a historical shift in dispersiveness among great speciator lineages during the evolutionary past. Here, we present a formalized framework that explains how repeated founder effects and shifting selection pressures on highly dispersive genotypes are the only ultimate causes needed to generate the paradox of the great speciators. Within this framework, we emphasize that lineage-specific traits and island-specific abiotic factors will result in varying levels of selection pressure against dispersiveness, caused by varying proximate eco-evolutionary mechanisms. Overall, we highlight how understanding patterns of diversification in the Ceyx dwarf kingfishers helped us generate a cohesive framework that provides a rigorous mechanistic explanation for patterns concordant with the paradox of the great speciators and the repeated emergence of geographic radiations in island archipelagoes across the globe.
-
Alba, Mar (Ed.)Abstract Adaptive radiations are characterised by the diversification and ecological differentiation of species, and replicated cases of this process provide natural experiments for understanding the repeatability and pace of molecular evolution. During adaptive radiation, genes related to ecological specialisation may be subject to recurrent positive directional selection. However, it is not clear to what extent patterns of lineage-specific ecological specialisation (including phenotypic convergence) are correlated with shared signatures of molecular evolution. To test this, we sequenced whole exomes from a phylogenetically dispersed sample of 38 murine rodent species, a group characterised by multiple, nested adaptive radiations comprising extensive ecological and phenotypic diversity. We found that genes associated with immunity, reproduction, diet, digestion and taste have been subject to pervasive positive selection during the diversification of murine rodents. We also found a significant correlation between genome-wide positive selection and dietary specialisation, with a higher proportion of positively selected codon sites in derived dietary forms (i.e. carnivores and herbivores) than in ancestral forms (i.e. omnivores). Despite striking convergent evolution of skull morphology and dentition in two distantly related worm-eating specialists, we did not detect more genes with shared signatures of positive or relaxed selection than in a non-convergent species comparison. While a small number of the genes we detected can be incidentally linked to craniofacial morphology or diet, protein-coding regions are unlikely to be the primary genetic basis of this complex convergent phenotype. Our results suggest a link between positive selection and derived ecological phenotypes, and highlight specific genes and general functional categories that may have played an integral role in the extensive and rapid diversification of murine rodents.more » « less
-
ABSTRACT Comparing patterns of performance and kinematics across behavior, development and phylogeny is crucial to understand the evolution of complex musculoskeletal systems such as the feeding apparatus. However, conveying 3D spatial data of muscle orientation throughout a feeding cycle, ontogenetic pathway or phylogenetic lineage is essential to understanding the function and evolution of the skull in vertebrates. Here, we detail the use of ternary plots for displaying and comparing the 3D orientation of muscle data. First, we illustrate changes in 3D jaw muscle resultants during jaw closing taxa the American alligator (Alligator mississippiensis). Second, we show changes in 3D muscle resultants of jaw muscles across an ontogenetic series of alligators. Third, we compare 3D resultants of jaw muscles of avian-line dinosaurs, including extant (Struthio camelus, Gallus gallus, Psittacus erithacus) and extinct (Tyrannosaurus rex) species to outline the reorganization of jaw muscles that occurred along the line to modern birds. Finally, we compare 3D resultants of jaw muscles of the hard-biting species in our sample (A. mississippiensis, T. rex, P. erithacus) to illustrate how disparate jaw muscle resultants are employed in convergent behaviors in archosaurs. Our findings show that these visualizations of 3D components of jaw muscles are immensely helpful towards identifying patterns of cranial performance, growth and diversity. These tools will prove useful for testing other hypotheses in functional morphology, comparative biomechanics, ecomorphology and organismal evolution.more » « less
-
Complex patterns of genome evolution associated with the end-Cretaceous [Cretaceous-Paleogene (K–Pg)] mass extinction limit our understanding of the early evolutionary history of modern birds. Here, we analyzed patterns of avian molecular evolution and identified distinct macroevolutionary regimes across exons, introns, untranslated regions, and mitochondrial genomes. Bird clades originating near the K–Pg boundary exhibited numerous shifts in the mode of molecular evolution, suggesting a burst of genomic heterogeneity at this point in Earth’s history. These inferred shifts in substitution patterns were closely related to evolutionary shifts in developmental mode, adult body mass, and patterns of metabolic scaling. Our results suggest that the end-Cretaceous mass extinction triggered integrated patterns of evolution across avian genomes, physiology, and life history near the dawn of the modern bird radiation.