Ancient DNA reveals elephant birds and kiwi are sister taxa and clarifies ratite bird evolution

Abstract

The evolution of the ratite birds has been widely attributed to vicariant speciation, driven by the Cretaceous breakup of the supercontinent Gondwana. The early isolation of Africa and Madagascar implies that the ostrich and extinct Madagascan elephant birds (Aepyornithidae) should be the oldest ratite lineages. We sequenced the mitochondrial genomes of two elephant birds and performed phylogenetic analyses, which revealed they are the closest relatives of the New Zealand kiwi, and distant from the basal ratite lineage of ostriches. This unexpected result strongly contradicts continental vicariance and instead supports flighted dispersal in all major ratite lineages. We suggest that convergence towards gigantism and flightlessness was facilitated by early Tertiary expansion into the diurnal herbivory niche following the extinction of the dinosaurs.One Sentence Summary: Ancient DNA reveals massive Madagascan elephant birds and tiny NZ kiwi are closest relatives, and supports flighted origin of ratites. Main Text:Despite extensive studies, the evolutionary history of the giant flightless ratite birds of the southern hemisphere landmasses, and the related flighted tinamous of South America, has remained a major unresolved question. The ratites and tinamous, termed palaeognaths due to their shared 'basal' palate structure, form the sister-taxon to all other living birds (neognaths). The living ratites are one of the few bird groups comprised largely of giant terrestrial herbivores and include: the emu and cassowary in Australia and New Guinea; kiwi in New Zealand; ostriches in Africa; and rhea in South America. In addition, two recently extinct groups included the largest birds known: the moa from New Zealand (1) [up to 2-3 m and 250 kg] and elephant birds from Madagascar [2-3 m height but up to 275 kg] (2, 3). Ratites have been believed to have originated through vicariant speciation driven by the continental breakup of Gondwana on the basis of congruence between the sequence of continental rifting and the presumed order of lineage divergence and distribution of ratites (4,5).New Zealand is the only landmass to have supported two major ratite lineages, the giant herbivorous moa and the chicken-sized, nocturnal, omnivorous kiwi. Morphological phylogenetic analyses initially suggested that these two groups were each other's closest relatives (6, 7), presumably diverging after the isolation of an ancestral form following the separation of New Zealand and Australia in the late Cretaceous ca. 80-60 million years ago (Ma) (8). However, subsequent studies suggest that kiwi are more closely related to the Australasian emu and cassowaries (9, 10), while the closest living relatives of the giant moa are the flighted South American tinamous (11-14). The latter relationship was completely unexpected on morphological grounds, and suggests a more complex evolutionary history than predicted by a model of strict vicariant speciation. By rendering ratites paraphyletic, the relationship between moa and tinamous also strong...

Comparative digesta retention patterns in ratites

“…This would mean that their ''intermediate'' gastrointestinal anatomy and physiology evolved recently from among ancestors that otherwise gave rise to birds of comparatively simple gastrointestinal tracts (Emus and Cassowaries: Cho et al 1984;Tinamous: Chikilian and De Speroni 1996;Kiwis: Potter et al 2006) and digestive physiology (this study for Emus), and as a sister group to the only extant flighted ratites. In contrast, the phylogeny based on mitochondrial sequences suggests that after the divergence of Ostriches from the ancestral ratite lineage, Rheas diverged next, with a common ancestor for all remaining ratite taxa (figure 3C in Mitchell et al 2014). This scenario matches the intermediate position of Rheas in terms of gastrointestinal anatomy, digesta retention, and gut volume.…”

“…For birds, characteristics of the gastrointestinal tract have been included in a large-scale morphology-based phylogeny reconstruction (Livezey and Zusi 2007) but represented only~0.5% (16 of 2945) of the characters used (Livezey and Zusi 2006). When compared to the 2 speciation models presented by Mitchell et al (2014), which are based on continental vicariance (i.e. assuming nonflighted dispersal that follows the sequence of the separation of landmasses from Gondwana) and a phylogeny based on mitochondrial sequence data, the digestive anatomy and physiology of ratites match the phylogeny-based model more parsimoniously than the continental vicariance model.…”

“…In both models, Ostriches separated first from the common ratite lineage, which corresponds to their most-derived gastrointestinal anatomy and physiology also documented in the present study. In the model of continental vicariance, Rheas are nested within the group consisting of Kiwis, Cassowaries, and Emus as a sister group to Tinamous (figure 3B in Mitchell et al 2014). This would mean that their ''intermediate'' gastrointestinal anatomy and physiology evolved recently from among ancestors that otherwise gave rise to birds of comparatively simple gastrointestinal tracts (Emus and Cassowaries: Cho et al 1984;Tinamous: Chikilian and De Speroni 1996;Kiwis: Potter et al 2006) and digestive physiology (this study for Emus), and as a sister group to the only extant flighted ratites.…”

“…), 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).…”

“…Various phylogenetic relationships among ratites have been proposed, differing specifically in whether Common Ostriches (Struthio camelus, hereafter Ostriches) or Rheas (Rhea spp.) are more closely related to Emus (Dromaius novaehollandiae; van Tuinen et al 1998, Cooper et al 2001, Haddrath and Baker 2001, Mitchell et al 2014). This phylogenetic debate also includes flighted Tinamous (Tinamou spp.…”