Deep-Time Demographic Inference Suggests Ecological Release as Driver of Neoavian Adaptive Radiation

Abstract

Assessing the applicability of theory to major adaptive radiations in deep time represents an extremely difficult problem in evolutionary biology. Neoaves, which includes 95% of living birds, is believed to have undergone a period of rapid diversification roughly coincident with the Cretaceous–Paleogene (K-Pg) boundary. We investigate whether basal neoavian lineages experienced an ecological release in response to ecological opportunity, as evidenced by density compensation. We estimated effective population sizes (Ne) of basal neoavian lineages by combining coalescent branch lengths (CBLs) and the numbers of generations between successive divergences. We used a modified version of Accurate Species TRee Algorithm (ASTRAL) to estimate CBLs directly from insertion–deletion (indel) data, as well as from gene trees using DNA sequence and/or indel data. We found that some divergences near the K-Pg boundary involved unexpectedly high gene tree discordance relative to the estimated number of generations between speciation events. The simplest explanation for this result is an increase in Ne, despite the caveats discussed herein. It appears that at least some early neoavian lineages, similar to the ancestor of the clade comprising doves, mesites, and sandgrouse, experienced ecological release near the time of the K-Pg mass extinction.

Data Types and the Phylogeny of Neoaves

“…Likewise, the fact that a doves + cuckoos clade recovered in analyses of coding data [11], UTRs [16], and transposable element insertions [32] could reflect gene flow involving those lineages. The hypothesis that ancient gene flow among neoavian stem lineages has an impact phylogenetic estimation could also explain the observation that clades IV and VI exhibit higher indel discordance than expected given the length of the branches uniting those clades [69]. Houde et al [69] interpreted the apparent elevation of indel discordance reflected incomplete lineage sorting and hypothesized that a transient increase in the effective population size led to a period of increased incomplete lineage sorting.…”

The Next Generation of Adaptive Radiation Studies in Plants

“…Ecological release can flatten and broaden fitness landscape peaks, which leads to increases in habitat or resource use and associated trait variation, as well as density compensation (Yoder et al 2010;Houde et al 2020). Another biological interaction is competition among close relatives, which is hypothesized to limit speciation during the asymptotic phase of the radiation (Yoder et al 2010).…”

Data Types and the Phylogeny of Neoaves

“…Likewise, the fact that a doves + cuckoos clade recovered in analyses of coding data [11], UTRs [16], and transposable element insertions [32] could reflect gene flow involving those lineages. The hypothesis that ancient gene flow among neoavian stem lineages has an impact phylogenetic estimation could also explain the observation that clades IV and VI exhibit higher indel discordance than expected given the length of the branches uniting those clades [66]. Houde et al [66] interpreted the apparent elevation of indel discordance reflected incomplete lineage sorting and hypothesized that a transient increase in the effective population size led to a period of increased incomplete lineage sorting.…”

“…The hypothesis that ancient gene flow among neoavian stem lineages has an impact phylogenetic estimation could also explain the observation that clades IV and VI exhibit higher indel discordance than expected given the length of the branches uniting those clades [66]. Houde et al [66] interpreted the apparent elevation of indel discordance reflected incomplete lineage sorting and hypothesized that a transient increase in the effective population size led to a period of increased incomplete lineage sorting. However, introgression would also lead to elevated indel discordance.…”