Phylogenomics and Morphology of Extinct Paleognaths Reveal the Origin and Evolution of the Ratites

Abstract

The Palaeognathae comprise the flightless ratites and the volant tinamous, and together with the Neognathae constitute the extant members of class Aves. It is commonly believed that Palaeognathae originated in Gondwana since most of the living species are found in the Southern Hemisphere [1-3]. However, this hypothesis has been questioned because the fossil paleognaths are mostly from the Northern Hemisphere in their earliest time (Paleocene) and possessed many putative ancestral characters [4]. Uncertainties regarding the origin and evolution of Palaeognathae stem from the difficulty in estimating their divergence times [1, 2] and their remarkable morphological convergence. Here, we recovered nuclear genome fragments from extinct elephant birds, which enabled us to reconstruct a reliable phylogenomic time tree for the Palaeognathae. Based on the tree, we identified homoplasies in morphological traits of paleognaths and reconstructed their morphology-based phylogeny including fossil species without molecular data. In contrast to the prevailing theories, the fossil paleognaths from the Northern Hemisphere were placed as the basal lineages. Combined with our stable divergence time estimates that enabled a valid argument regarding the correlation with geological events, we propose a new evolutionary scenario that contradicts the traditional view. The ancestral Palaeognathae were volant, as estimated from their molecular evolutionary rates, and originated during the Late Cretaceous in the Northern Hemisphere. They migrated to the Southern Hemisphere and speciated explosively around the Cretaceous-Paleogene boundary. They then extended their distribution to the Gondwana-derived landmasses, such as New Zealand and Madagascar, by overseas dispersal. Gigantism subsequently occurred independently on each landmass.

How do seemingly non-vagile clades accomplish trans-marine dispersal? Trait and dispersal evolution in the landfowl (Aves: Galliformes)

“…Extinction of the original vagile ancestor lineages over time may then result in the appearance of dispersal-limited groups with relict distributions. This cycle of range expansion, morphological evolution and extinction has recently been favoured to explain the distributions of non-vagile birds as diverse as the flightless ratites and tinamous [5,7,8], and the mostly flightless New Zealand wrens [16]. However, in these cases, the putative vagile ancestors were purely hypothetical.…”

“…However, in these cases, the putative vagile ancestors were purely hypothetical. The only fossil evidence of vagile ratites is from the Palaearctic, where no extant ratites reside [8,[17][18][19]. Similarly, all known fossil New Zealand wrens already feature non-vagile traits [16].…”

“…For example, large-bodied and flightless ratite birds (e.g. ostrich, emu) have seemingly colonized distant areas over evolutionary time despite severe dispersal constraints [5][6][7][8].…”

Cretaceous origin of giant rhinoceros beetles (Dynastini; Coleoptera) and correlation of their evolution with the Pangean breakup

“…Indeed, the correlations between continental drift and phylogenetic branching patterns of terrestrial animals such as Eutherian mammals (Nishihara et al, 2009;dos Reis et al, 2012), Palaeognathae (ratite and tinamou: Cooper et al, 2001;Haddrath and Baker, 2012;Yonezawa et al, 2017), Pleurodira (side-necked turtle: Vargas-Ramírez et al, 2008), Anura (frogs: Bossuyt et al, 2006), Cichlidae (cichlid fish: Friedman et al, 2013) and Plecoptera (stoneflies: McCulloch et al, 2016) have been vigorously argued. Some of these studies (e.g., Haddrath and Baker, 2012;dos Reis et al, 2012;Yonezawa et al, 2017) suggested that biogeographical distribution patterns were not necessarily established merely by continental drift, but that the overseas 'sweepstakes dispersal route' (Simpson, 1940) should be considered.…”

“…Some of these studies (e.g., Haddrath and Baker, 2012;dos Reis et al, 2012;Yonezawa et al, 2017) suggested that biogeographical distribution patterns were not necessarily established merely by continental drift, but that the overseas 'sweepstakes dispersal route' (Simpson, 1940) should be considered. A sweepstakes dispersal route is "a possible route of faunal interchange which is unlikely to be used by most animals, but which will, by chance, be used by some" (Allaby, 1999).…”