Craniofacial development illuminates the evolution of nightbirds (Strisores)

Evolutionary variation in ontogeny played a central role in the origin of the avian skull. However, its influence in subsequent bird evolution is largely unexplored. We assess the links between ontogenetic and evolutionary variation of skull morphology in Strisores (nightbirds). Nightbirds span an exceptional range of ecologies, sizes, life-history traits and craniofacial morphologies constituting an ideal test for evo-devo hypotheses of avian craniofacial evolution. These morphologies include superficially ‘juvenile-like’ broad, flat skulls with short rostra and large orbits in swifts, nightjars and allied lineages, and the elongate, narrow rostra and globular skulls of hummingbirds. Here, we show that nightbird skulls undergo large ontogenetic shape changes that differ strongly from widespread avian patterns. While the superficially juvenile-like skull morphology of many adult nightbirds results from convergent evolution, rather than paedomorphosis, the divergent cranial morphology of hummingbirds originates from an evolutionary reversal to a more typical avian ontogenetic trajectory combined with accelerated ontogenetic shape change. Our findings underscore the evolutionary lability of cranial growth and development in birds, and the underappreciated role of this aspect of phenotypic variability in the macroevolutionary diversification of the amniote skull.

SLC2A12 of SLC2 Gene Family in Bird Provides Functional Compensation for the Loss of SLC2A4 Gene in Other Vertebrates

Avian genomes are small and lack some genes that are conserved in the genomes of most other vertebrates including nonavian sauropsids. One hypothesis stated that paralogs may provide biochemical or physiological compensation for certain gene losses; however, no functional evidence has been reported to date. By integrating evolutionary analysis, physiological genomics, and experimental gene interference, we clearly demonstrate functional compensation for gene loss. A large-scale phylogenetic analysis of over 1,400 SLC2 gene sequences identifies six new SLC2 genes from nonmammalian vertebrates and divides the SLC2 gene family into four classes. Vertebrates retain class III SLC2 genes but partially lack the more recent duplicates of classes I and II. Birds appear to have completely lost the SLC2A4 gene that encodes an important insulin-sensitive GLUT in mammals. We found strong evidence for positive selection, indicating that the N-termini of SLC2A4 and SLC2A12 have undergone diversifying selection in birds and mammals, and there is a significant correlation between SLC2A12 functionality and basal metabolic rates in endotherms. Physiological genomics have uncovered that SLC2A12 expression and allelic variants are associated with insulin sensitivity and blood glucose levels in wild birds. Functional tests have indicated that SLC2A12 abrogation causes hyperglycemia, insulin resistance, and high relative activity, thus increasing energy expenditures that resemble a diabetic phenotype. These analyses suggest that the SLC2A12 gene not only functionally compensates insulin response for SLC2A4 loss but also affects daily physical behavior and basal metabolic rate during bird evolution, highlighting that older genes retain a higher level of functional diversification.

Anatomy of Parahesperornis: Evolutionary Mosaicism in the Cretaceous Hesperornithiformes (Aves)

The Hesperornithiformes constitute the first known avian lineage to secondarily lose flight in exchange for the evolution of a highly derived foot-propelled diving lifestyle, thus representing the first lineage of truly aquatic birds. First unearthed in the 19th century, and today known from numerous Late Cretaceous (Cenomanian-Maastrichtian) sites distributed across the northern hemisphere, these toothed birds have become icons of early avian evolution. Initially erected as a taxon in 1984 by L. D. Martin, Parahesperornis alexi is known from the two most complete hesperornithiform specimens discovered to date and has yet to be fully described. P. alexi thus contributes significantly to our understanding of hesperornithiform birds, despite often being neglected in favor of the iconic Hesperornis. Here, we present a full anatomical description of P. alexi based upon the two nearly complete specimens in the collections of the University of Kansas Natural History Museum, as well as an extensive comparison to other hesperornithiform taxa. This study reveals P. alexi to possess a mosaic of basal and derived traits found among other hesperornithiform taxa, indicating a transitional form in the evolution of these foot-propelled diving birds. This study describes broad evolutionary patterns within the Hesperornithiformes, highlighting the significance of these birds as not only an incredible example of the evolution of ecological specializations, but also for understanding modern bird evolution, as they are the last known divergence of pre-modern bird diversification.

A Bird's-Eye View of Pollination: Biotic Interactions as Drivers of Adaptation and Community Change

Nectarivorous birds and bird-pollinated plants are linked by a network of interactions. Here I ask how these interactions influence evolution and community composition. I find near complete evidence for the effect of birds on plant evolution. Experiments show the process in action—birds select among floral phenotypes in a population—and comparative studies find the resulting pattern—bird-pollinated species have long-tubed, red flowers with large nectar volumes. Speciation is accomplished in one “magical” step when adaptation for bird pollination brings about divergent morphology and reproductive isolation. In contrast, evidence that plants drive bird evolution is fragmentary. Studies of selection on population-level variation are lacking, but the resulting pattern is clear—nectarivorous birds have evolved a remarkable number of times and often have long bills and brush-tipped or tubular tongues. At the level of the ecological guild, birds select among plant species via an effect on seed set and thus determine plant community composition. Plants simultaneously influence the relative fitness of bird species and thus determine the composition of the bird guild. Interaction partners may give one guild member a constant fitness advantage, resulting in competitive exclusion and community change, or may act as limiting resources that depress the fitness of frequent species, thus stabilizing community composition and allowing the coexistence of diversity within bird and plant guilds.

Functional Evolution of Avian RIG-I-Like Receptors

RIG-I-like receptors (retinoic acid-inducible gene-I-like receptors, or RLRs) are family of pattern-recognition receptors for RNA viruses, consisting of three members: retinoic acid-inducible gene I (RIG-I), melanoma differentiation-associated gene 5 (MDA5) and laboratory of genetics and physiology 2 (LGP2). To understand the role of RLRs in bird evolution, we performed molecular evolutionary analyses on the coding genes of avian RLRs using filtered predicted coding sequences from 62 bird species. Among the three RLRs, conservation score and dN/dS (ratio of nonsynonymous substitution rate over synonymous substitution rate) analyses indicate that avian MDA5 has the highest conservation level in the helicase domain but a lower level in the caspase recruitment domains (CARDs) region, which differs from mammals; LGP2, as a whole gene, has a lower conservation level than RIG-I or MDA5. We found evidence of positive selection across all bird lineages in RIG-I and MDA5 but only on the stem lineage of Galliformes in LGP2, which could be related to the loss of RIG-I in Galliformes. Analyses also suggest that selection relaxation may have occurred in LGP2 during the middle of bird evolution and the CARDs region of MDA5 contains many positively selected sites, which might explain its conservation level. Spearman’s correlation test indicates that species-to-ancestor dN/dS of RIG-I shows a negative correlation with endogenous retroviral abundance in bird genomes, suggesting the possibility of interaction between immunity and endogenous retroviruses during bird evolution.

The soft explosive model of placental mammal evolution

Recent molecular dating estimates for placental mammals echo fossil inferences for an explosive interordinal diversification, but typically place this event some 10-20 million years earlier than the Paleocene fossils, among apparently more “primitive” mammal faunas. However, current models of molecular evolution do not adequately account for parallel rate changes, and result in dramatic divergence underestimates for large, long-lived mammals such as whales and hominids. Calibrating among these taxa shifts the rate model errors deeper in the tree, inflating interordinal divergence estimates. We employ simulations based on empirical rate variation, which show that this “error-shift inflation” can explain previous molecular dating overestimates relative to fossil inferences. Molecular dating accuracy is substantially improved in the simulations by focusing on calibrations for taxa that retain plesiomorphic life-history characteristics. Applying this strategy to the empirical data favours the soft explosive model of placental evolution, in line with traditional palaeontological interpretations – a few Cretaceous placental lineages give rise to a rapid interordinal diversification following the 66 Ma Cretaceous-Paleogene boundary mass extinction. Our soft explosive model for the diversification of placental mammals brings into agreement previously incongruous molecular, fossil, and ancestral life history estimates, and closely aligns with a growing consensus for a similar model for bird evolution. We show that recent criticism of the soft explosive model relies on ignoring both experimental controls and statistical confidence, as well as misrepresentation, and inconsistent interpretations of morphological phylogeny. More generally, we suggest that the evolutionary properties of adaptive radiations may leave current molecular dating methods susceptible to overestimating the timing of major diversification events.