Convergent evolution of bird-mammal shared characteristics for adapting to nocturnality

Abstract

The diapsid lineage (birds) and synapsid lineage (mammals), share a suite of functionally similar characteristics (e.g., endothermy) that are considered to be a result of their convergent evolution, but the candidate selections leading to this convergent evolution are still under debates. Here, we used a newly developed molecular phyloecological approach to reconstruct the diel activity pattern of the common ancestors of living birds. Our results strongly suggest that they had adaptations to nocturnality during their early evolution, which is remarkably similar to that of ancestral mammals. Given their similar adaptation to nocturnality, we propose that the shared traits in birds and mammals may have evolved as a result of the convergent evolution of their early ancestors adapting to ecological factors (e.g., low ambient temperature) associated with nocturnality. Finally, a conceptually unifying ecological model on the evolution of endothermy in diverse organisms with an emphasis on low ambient temperature is proposed. We reason that endothermy may evolve as an adaptive strategy to enable organisms to effectively implement various life cycle activities under relatively low-temperature environments. In particular, a habitat shift from high-temperature to relatively low-temperature environments is identified as a common factor underlying the evolution of endothermy.

Molecular phyloecology suggests a trophic shift concurrent with the evolution of the first birds

“…The functions of these digestive system-related genes are relatively well-studied and are known to play important roles in the digestion and absorption of carbohydrates, proteins, and fats. Following the molecular phyloecological approach to reconstruct ancestral traits [30][31][32] , we used branch and branch-site models implemented in PAML software 33 to detect positively selected genes (PSGs) along our target branches, and PSGs were found based on branch-site model (Table 1). The evidence of the positive selection of genes may suggest a functional enhancement of their corresponding functions in relevant lineages [30][31][32] .…”

“…1 Phylogeny and the diets of modern birds. Phylogenetic relationships of taxa used follow published studies 30,[138][139][140][141][142][143] . Dietary categories of each bird species follow one published study 145 and are shown in different colors, and the bird species without dietary information available are shown in black.…”

“…This is particularly the case for ancestral birds, as they evolve toward miniaturization suitable for powered flight 95,96 and their small body size may be particularly vulnerable to predators. More importantly, their evolution of endothermy and powered flight requires much more energy and, consequently, frequent foraging 3,5,30,97 . Frequent foraging may have, most often, exposed them to predators, hence leading to their high predation risk.…”

“…In support of this, fossil evidence shows that ancestral birds, such as enantiornithines and Confuciusornis, have a precocial development style 5,6,98 , although there is an evolutionary transition of a reduced precocity in ornithurine birds 99 and precocity is generally considered to be an anti-predation strategy for facing historically strong predation pressure 100,101 . Moreover, one recent study shows that the CALB was probably cathemeral (i.e., active in both day and night), and that it may have evolved an enhanced visual capability to detect motion 30 . Cathemerality is considered to be linked to high predation risk 102,103 and the promoted motion detection ability of the CALB may mainly help to detect approaching predators 104 given its herbivory.…”

“…The recent development of a molecular phyloecological approach, which employs the phylogenetic evolutionary analyses of the molecular markers indicative of trait states, allows us to reconstruct ancestral traits using molecular data [30][31][32] . The substantial dietary differences between carnivores and herbivores in terms of the amounts of dietary components (e.g., carbohydrates, proteins, and fats) 17,23,25,27 , and the adaptation of digestive system-related genes to the variations of dietary components of animals 16,17,[23][24][25][26]29 may suggest that digestive system-related genes can be used as the molecular markers of diets to reconstruct the diets of ancestral animals in the context of molecular phyloecology 29 .…”