Phylogenomic evidence for multiple losses of flight in ratite birds

Abstract

Ratites (ostriches, emus, rheas, cassowaries, and kiwis) are large, flightless birds that have long fascinated biologists. Their current distribution on isolated southern land masses is believed to reflect the breakup of the paleocontinent of Gondwana. The prevailing view is that ratites are monophyletic, with the flighted tinamous as their sister group, suggesting a single loss of flight in the common ancestry of ratites. However, phylogenetic analyses of 20 unlinked nuclear genes reveal a genome-wide signal that unequivocally places tinamous within ratites, making ratites polyphyletic and suggesting multiple losses of flight. Phenomena that can mislead phylogenetic analyses, including long branch attraction, base compositional bias, discordance between gene trees and species trees, and sequence alignment errors, have been eliminated as explanations for this result. The most plausible hypothesis requires at least three losses of flight and explains the many morphological and behavioral similarities among ratites by parallel or convergent evolution. Finally, this phylogeny demands fundamental reconsideration of proposals that relate ratite evolution to continental drift.convergence ͉ flightlessness ͉ Paleognath ͉ homoplasy ͉ vicariance biogeography

Twenty-first century advances in knowledge of the biology of moa (Aves: Dinornithiformes): a new morphological analysis and moa diagnoses revised

“…Their analysis included protocols to account for rates-across-sites heterogeneity by use of specific partitioning models of sequence evolution among protein coding positions and RNA structures and, unlike in previous studies of mitochondrial DNA, ratite monophyly was not enforced. Their favoured analysis confirmed the topology found by Harshman et al (2008), in which ostriches were basal and tinamous embedded among ratites. However, they found tinamous to be very strongly supported as sister to moa and this combined clade sister to Australasian ratites.…”

“…Therefore, we will only compare our tree in detail to that of Phillips et al (2010) who, like us, used a range of neognaths to root their tree. As was first indicated by Hackett et al (2008) and Harshman et al (2008), Phillips et al (2010) found tinamous made ratites paraphyletic, and specifically were strongly supported as sister to moa. This appears to contrast greatly from our finding in Analysis 1 that tinamous constituted a basal branch in palaeognaths.…”

“…It is clear that developing analysis protocols, more comprehensive datasets and variations in species composition will affect interpretations of relationships for some time to come. However, as the current most comprehensive analyses, the Phillips et al (2010) and Harshman et al (2008) studies suggest that flight has been independently lost several times among palaeognath lineages. Moreover, in a revised evolutionary timescale for palaeognaths, moa and tinamous were estimated to have diverged about 60 Ma at about the same time as kiwi did from casuariids.…”

“…Exemplary among such works was that of Hackett et al (2008) which used 20 unlinked nuclear loci to explore the phylogenetic relationships of the avian radiation. Harshman et al (2008) developed the dataset Hackett et al (2008) used to explore palaeognath relationships. They found unequivocal support for tinamous to be nested within ratites with ostrich sister to remaining palaeognaths.…”

Comparative digesta retention patterns in ratites

“…), Kiwis (Apteryx spp. ), Moas, and Elephant birds; the debate is relevant to whether flightlessness in ratites evolved only once or several times independently (Harshman et al 2008, Phillips et al 2010, Baker et al 2014. Most recent results indicate a discrepancy between geographic location and phylogenetic relatedness among ratite species, suggesting that the major ratite lineages must have dispersed by flying before evolving converging anatomical characteristics and flightlessness (Mitchell et al 2014).…”