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The Evolution and Fossil Record of Palaeognathous Birds (Neornithes: Palaeognathae)



The extant diversity of the avian clade Palaeognathae is composed of the iconic flightless ratites (ostriches, rheas, kiwi, emus, and cassowaries), and the volant tinamous of Central and South America. Palaeognaths were once considered a classic illustration of diversification driven by Gondwanan vicariance, but this paradigm has been rejected in light of molecular phylogenetic and divergence time results from the last two decades that indicate that palaeognaths underwent multiple relatively recent transitions to flightlessness and large body size, reinvigorating research into their evolutionary origins and historical biogeography. This revised perspective on palaeognath macroevolution has highlighted lingering gaps in our understanding of how, when, and where extant palaeognath diversity arose. Towards resolving those questions, we aim to comprehensively review the known fossil record of palaeognath skeletal remains, and to summarize the current state of knowledge of their evolutionary history. Total clade palaeognaths appear to be one of a small handful of crown bird lineages that crossed the Cretaceous-Paleogene (K-Pg) boundary, but gaps in their Paleogene fossil record and a lack of Cretaceous fossils preclude a detailed understanding of their multiple transitions to flightlessness and large body size, and recognizable members of extant subclades generally do not appear until the Neogene. Despite these knowledge gaps, we combine what is known from the fossil record of palaeognaths with plausible divergence time estimates, suggesting a relatively rapid pace of diversification and phenotypic evolution in the early Cenozoic. In line with some recent authors, we surmise that the most recent common ancestor of palaeognaths was likely a relatively small-bodied, ground-feeding bird, features that may have facilitated total-clade palaeognath survivorship through the K-Pg mass extinction, and which may bear on the ecological habits of the ancestral crown bird.
Diversity 2022, 14, 105.
The Evolution and Fossil Record of Palaeognathous Birds
(Neornithes: Palaeognathae)
Klara Widrig
* and Daniel J. Field
Department of Earth Sciences, University of Cambridge, Cambridge CB2 7EQ, UK
Museum of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK
* Correspondence: (K.W.); (D.J.F.); Tel.: +44-(0)1223-768329 (D.J.F.)
Abstract: The extant diversity of the avian clade Palaeognathae is composed of the iconic flightless
ratites (ostriches, rheas, kiwi, emus, and cassowaries), and the volant tinamous of Central and South
America. Palaeognaths were once considered a classic illustration of diversification driven by Gond-
wanan vicariance, but this paradigm has been rejected in light of molecular phylogenetic and diver-
gence time results from the last two decades that indicate that palaeognaths underwent multiple
relatively recent transitions to flightlessness and large body size, reinvigorating research into their
evolutionary origins and historical biogeography. This revised perspective on palaeognath macro-
evolution has highlighted lingering gaps in our understanding of how, when, and where extant
palaeognath diversity arose. Towards resolving those questions, we aim to comprehensively review
the known fossil record of palaeognath skeletal remains, and to summarize the current state of
knowledge of their evolutionary history. Total clade palaeognaths appear to be one of a small hand-
ful of crown bird lineages that crossed the Cretaceous-Paleogene (K-Pg) boundary, but gaps in their
Paleogene fossil record and a lack of Cretaceous fossils preclude a detailed understanding of their
multiple transitions to flightlessness and large body size, and recognizable members of extant sub-
clades generally do not appear until the Neogene. Despite these knowledge gaps, we combine what
is known from the fossil record of palaeognaths with plausible divergence time estimates, suggest-
ing a relatively rapid pace of diversification and phenotypic evolution in the early Cenozoic. In line
with some recent authors, we surmise that the most recent common ancestor of palaeognaths was
likely a relatively small-bodied, ground-feeding bird, features that may have facilitated total-clade
palaeognath survivorship through the K-Pg mass extinction, and which may bear on the ecological
habits of the ancestral crown bird.
Keywords: Palaeognathae; ostrich; tinamou; ratite; emu; kiwi; moa; elephant bird; rhea; Lithorn-
1. Introduction
Crown birds (Neornithes) comprise roughly 11,000 extant species [1]. They are di-
vided into the reciprocally monophyletic Palaeognathae and Neognathae, with the latter
including the hyperdiverse clade Neoaves [1]. At no point in time do total group palaeog-
naths appear to have been particularly diverse, especially in comparison with contempo-
raneous neognath diversity. Despite their relatively sparse taxonomic diversity, however,
the position of palaeognaths as the sister group to all other neornithines makes them crit-
ical to efforts to understand the early evolutionary history of crown birds. Palaeognathae
is diagnosed by several traits including a unique palatal structure characterized by en-
larged basipterygoid processes and fused pterygoids and palatines (Figure 1), a grooved
rhamphotheca, a single articular facet for the otic capitulum of the quadrate, and open
ilioischiadic foramina (Figure 2) [2–6]. The palatal structure of palaeognaths was tradi-
tionally considered plesiomorphic for Neornithes [7], though recent evidence regarding
Citation: Widrig, K.; Field, D.J. The
Evolution and Fossil Record of Pal-
aeognathous Birds (Neornithes: Pal-
aeognathae). Diversity 2022, 14, 105.
Academic Editors: Michael Wink,
Eric Buffetaut and Delphine Angst
Received: 31 December 2021
Accepted: 27 January 2022
Published: 1 February 2022
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Copyright: © 2022 by the authors. Li-
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Diversity 2022, 14, 105 2 of 70
the palatal structure of the near-crown Ichthyornithes may indicate that the palaeogna-
thous palate is in fact a synapomorphy of Palaeognathae [8,9].
Figure 1. Comparison of the palate of a palaeognathous and a neognathous bird. (a) Palate of the
palaeognathous Emu Dromaius novaehollandiae. The basipterygoid process is elongate, and the pter-
ygoid and palatine are fused (demarcation between them is approximate). (b) Palate of the neogna-
thous Mute Swan Cygnus olor. The pterygoid and palatine are connected by an intrapterygoid joint,
and the short basipterygoid processes are mostly obscured by the pterygoids.
Extant palaeognaths are represented by 46 species of tinamou (Tinamidae) and two
species of rhea (Rheidae) in Central and South America, two species of ostrich (Struthi-
onidae) in Africa, the monotypic emu and three species of cassowaries (Casuariidae) in
Australia and New Guinea, and approximately five species of kiwi in New Zealand (Ap-
terygidae) [10]. Nine species of moa (Dinornithiformes) [11] and four species of elephant
bird (Aepyornithidae) [12] survived into the Holocene in New Zealand and Madagascar
respectively, before their extinction which may have been related to human activity that
had a disproportionate impact on insular flightless birds [13].
Diversity 2022, 14, 105 3 of 70
Figure 2. Comparison of the pelvis of a palaeognathous and a neognathous bird. The ilioischiadic
foramen is highlighted in blue. (a) Pelvis of the Little Spotted Kiwi Apteryx owenii. The ilium and
ischium are unfused throughout their lengths, leaving the ilioischiadic foramen open. (b) Pelvis of
the Mute Swan Cygnus olor. The ilioischiadic foramen is closed due to the fusion of the posterior
ilium and ischium.
Despite being relatively species-poor, extant and recently extinct palaeognaths en-
compass an impressive range of body sizes and ecologies. The group contains both curso-
rial open habitat specialists (e.g., emu) and graviportal forest dwellers (e.g., cassowaries),
and feeding strategies ranging from cryptic nocturnal invertivores (e.g., kiwi) to megaher-
bivorous browsers (e.g., moa). Out of all extant palaeognaths, only tinamous (Tinamidae)
are capable of flight [14]. This clade comprises small to medium-sized birds, ranging from
43 g in the smallest species (the Dwarf Tinamou Taoniscus nanus) [15], to 2080 g in the
Diversity 2022, 14, 105 4 of 70
largest females of the Gray Tinamou (Tinamus tao) [16]. By contrast, flightless palaeog-
naths, from here on referred to collectively as “ratites” (acknowledging the paraphyletic
nature of the group), are renowned for their gigantism. The Common Ostrich Struthio
camelus is the world’s largest extant bird in both height and weight, with large males
reaching sizes up to 2.8 m and 156 kg [17]. Recently extinct ratites were even larger: A
body mass of 860 kg was estimated from femur measurements of an exceptionally large
individual of the elephant bird Vorombe titan, making this species the heaviest-known bird
ever discovered [12]. Females of the moa Dinornis robustus were less massive but appear
to have constituted the tallest birds yet discovered, attaining heights of 3.6 m [18,19].
Several early authors argued that ‘ratites’ represented a non-monophyletic assem-
blage of large-bodied, flightless birds, and debate regarding the potential non-monophyly
of ratites persisted through much of the 20th Century [4,20–24]. Opinion shifted with the
widespread acceptance of continental drift theory in the latter half of the 20th century, as
a monophyletic “Ratitae” became enshrined as a classic example of Gondwanan vicari-
ance biogeography, a hypothesis stipulating that stem group ratites became flightless
prior to the breakup of Gondwana, and that Gondwanan fragmentation drove the diver-
gence of the extant ratite lineages as populations became geographically isolated from
one-another [25–27]. This hypothesis of a monophyletic “Ratitae”, sister to Tinamidae,
was supported by a number of phenotypic features such as the absence of a triosseal canal
and sternal keel, and the presence of a fused scapulocoracoid (Figure 3) [5]. Indeed, the
term “ratite” refers to the flat, raft-like sterna of taxa lacking a sternal keel (Figure 4) [28].
This consensus opinion was upheld for several decades by most phylogenetic analyses of
morphological characters [29–31], though analyses of cranial characters recovered alter-
native relationships [32–34]. However, over the past twenty years, molecular phylogenetic
analyses have forced a wholescale revision of the Gondwanan vicariance paradigm of pal-
aeognath evolution and historical biogeography. Evidence from analyses of both nuclear
[35–43] and mitochondrial DNA [41,42,44–46], as well as large-scale phylogenomic anal-
yses [47–50], demonstrate that tinamids are in fact phylogenetically nested within ratites,
rendering “Ratitae” paraphyletic, once again reviving the early hypothesis of ratite non-
monophyly [4,20–24] (Figure 5).
Figure 3. Comparison of the shoulder girdle of a flightless palaeognath displaying the fused ‘ratite’
condition, and that of a volant palaeognath in left lateral view. (a) Fused scapulocoracoid of the
flightless Greater Rhea Rhea americana. (b) Unfused scapula and coracoid of the volant Andean Tin-
amou Nothoprocta pentlandii.
Diversity 2022, 14, 105 5 of 70
Figure 4. Comparison of the sterna of a flightless palaeognath, the Common Ostrich Struthio camelus
and a volant palaeognath, the Andean Tinamou Nothoprocta pentlandii. (a) Sternum of S. camelus in
dorsal view. (b) Sternum of S. camelus in left lateral view. A sternal keel is absent. (c) Sternum of N.
pentlandii in dorsal view. (d) Sternum of N. pentlandii in left lateral view. A deep sternal keel provides
an attachment area for the pectoralis and supracoracoideus muscles.
Figure 5. Old and new hypotheses of palaeognath interrelationships. Extinct clades are indicated by
†. (a) Ratite monophyly based on the morphological study of Livezey and Zusi [30]. (b) Molecular
phylogeny suggesting ratite paraphyly recovered by Mitchell, et al. [45], Grealy, et al. [41],
Yonezawa, et al. [49], Urantówka , et al. [46], and Almeida, et al. [42].
The most parsimonious interpretation of this revised tree topology would be that the
most recent common ancestor of crown Palaeognathae was flightless, with a reacquisition
Diversity 2022, 14, 105 6 of 70
of flight arising along the tinamou stem lineage. This interpretation is indeed favoured by
maximum likelihood analyses [44] and cannot be definitively rejected; however, this hy-
pothesis would seem to be unlikely from first principles (after all, strong evidence exists
for only four independent acquisitions of powered flight throughout the entire evolution-
ary history of animals [51]). By contrast, multiple independent transitions to flightlessness
within the same crown bird subclade are not uncommon. For example, flightlessness has
arisen dozens of times in Rallidae among island-dwelling taxa [52,53]. According to some
recent molecular topologies, transitions to flightlessness arose a minimum of six times in
palaeognaths, and transitions to gigantism a minimum of five [41,45].
The recent revival of a phylogenetic hypothesis stipulating that ratites repeatedly and
independently lost the capacity to fly has largely been driven by molecular phylogenetic
analyses [36–46,48–50,54–58], but has accrued supporting evidence from independent da-
tasets. For instance, embryological studies have demonstrated important differences in
patterns of wing growth among ostriches and emu, suggesting that alternative hetero-
chronic mechanisms may underlie the acquisition of flightlessness in disparate ratite taxa
and potentially supporting independent evolutionary transitions to flightlessness among
ratites [59]. Furthermore, misexpression of the cardiac transcription factor Nkx2.5 is asso-
ciated with reduced wing growth in chicken embryos, and this transcription factor is ex-
pressed in the wings of emu embryos but not ostriches—again indicating the potential
non-homology of flightlessness in emu and ostriches [60]. Sackton, et al. [50] found that
many similarities in ratite forelimb morphology may be the result of convergence in gene
regulatory networks, rather than the product of homologous changes to protein coding
genes. Overall, the existing body of evidence is congruent with the hypothesis that ‘ratites’
are indeed paraphyletic, and have repeatedly converged on a suite of remarkably similar
morphologies that were long interpreted as synapomorphies for the group. Much remains
to be understood about the underlying drivers of these independent transitions to large
size and flightlessness, as well as the developmental underpinnings of convergent ratite
The recognition of ratite paraphyly, coupled with phylogenomic time trees that indi-
cate an origin of crown palaeognaths long after the breakup of Gondwana commenced
(e.g., [41,42,45,48,49,55]), makes the classic vicariance hypothesis untenable. Instead, pre-
sent-day palaeognath biogeography must be the product of dispersal of volant ancestral
palaeognaths to multiple landmasses preceding independent origins of flightlessness
(Figure 6). However, this interpretation raises many questions regarding the nature of the
volant last common ancestor of crown palaeognaths. Tinamous are the only extant volant
palaeognaths available for reference, but they are primarily ground-dwelling and are only
capable of flight over relatively short distances to flee predators or roost in trees [14,61]. It
is difficult to imagine a burst-flying tinamou-like bird undertaking the transoceanic jour-
neys needed to explain the distribution of extant palaeognaths (Figure 6), thus they would
appear to be a poor analogue for hypothetical dispersive ancestral palaeognaths. Fossil
evidence further suggests that the specialized burst flying of extant tinamous was not ple-
siomorphic for palaeognaths. The extinct lithornithids (Lithornithidae), known from the
Paleocene and Eocene of Europe and North America, were apparently volant and appear
to represent the oldest and most stemward known total-clade palaeognaths [49,62–65].
Importantly, they also appear to have been more capable long-distance fliers than extant
tinamids are [62,65], and, as the earliest known palaeognaths in the fossil record, they may
provide the best models for informing reconstructions of the dispersive ancestral palaeog-
naths that gave rise to extant palaeognath diversity.
Diversity 2022, 14, 105 7 of 70
Figure 6. Present-day geographic ranges of extant palaeognath subclades. Range of Rheidae in dark
blue, Tinamidae in orange, Struthionidae in green, Casuariidae in aqua, and Apterygidae in pink.
In order to probe deeper into the origin and early evolution of total group Palaeog-
nathae, an in-depth understanding of the palaeognath fossil record is necessary. Early fos-
sil palaeognaths are rare, and the phylogenetic interrelationships among them are poorly
understood. For example, the monophyly and phylogenetic position of lithornithids are
debated, and thus their relevance for clarifying the pattern and timing of the extant pal-
aeognath radiation remains unclear. Due to the phylogenetic position of palaeognaths as
the extant sister taxon of all other Neornithes, stem palaeognaths, which may include
lithornithids, should provide key insight into the nature of the ancestral crown bird. Re-
cent time-scaled phylogenies suggest that total-group palaeognaths were one of just a
small number of extant neornithine lineages that passed through the Cretaceous-Paleo-
gene (K-Pg) mass extinction event (e.g. [48,69–72]). A better understanding of the ecology
and biology of early stem palaeognaths could therefore help clarify the biological attrib-
utes of avian survivors of the end-Cretaceous mass extinction, which appears to have
eliminated all non-neornithine avialans [73]. Early palaeognath fossils from around the
world will also be critical for illustrating how the remarkable convergent evolution of
flightlessness and gigantism arose among crown palaeognaths, as well as providing in-
sight into the biogeographic origins of extant palaeognath subclades and their responses
to Cenozoic shifts in climate and environment [74,75].
Here, we summarize the current state of knowledge regarding the palaeognath fossil
record. Useful reviews on palaeognath fossils and the evolutionary history of this group
have previously been published, e.g. [76–78], and we refer interested readers to these ex-
cellent summaries, but the present review is the first attempt to systematically address the
fossil record of palaeognaths in its entirety. We present the most specific locality data re-
ported in the literature for each fossil occurrence, necessarily limited by the differential
specificity available for certain records. We outline key lingering gaps in the known pal-
aeognath fossil record, and suggest potential ways forward in hopes of narrowing those
gaps. In addition, we provide an overview of strong inferences about palaeognath macro-
evolution that can be made on the basis of current molecular phylogenies and estimated
divergence times, and summarise what can be reasonably inferred about the most recent
common ancestor of crown group palaeognaths. We hope that this review provides both
a solid base of information for those interested in the evolution and fossil record of pal-
aeognaths, and helps inspire further work clarifying the evolutionary history of these re-
markable birds.
Diversity 2022, 14, 105 8 of 70
Institutional abbreviations are as follows: AM–Australian Museum, Darlinghurst,
Australia; AIM–Auckland Institute and Museum, Auckland, New Zealand; AMNH–
American Museum of Natural History, New York, New York, USA; AU–Auckland Uni-
versity, Auckland, New Zealand; AUG–Aristotle University School of Geology, Thessalo-
niki, Greece; BGR–Bundesanstalt für Geowissenschaften Und Rohstoffe, Hanover, Ger-
many; CICYTTP–Centro de Investigación Científica y de Transferencia Tecnológica a la
Producción, Diamante, Argentina; CPC–Commonwealth Palaeontological Collections,
Canberra, Australia; DK–Danekrae collections, Geological Museum, University of Copen-
hagen, Copenhagen, Denmark; FMNH–Field Museum of Natural History, Chicago, Illi-
nois, USA; GHUNLP–Universidad Nacional de La Pampa, Santa Rosa, Argentina; GMB–
Geological Museum of Budapest, Budapest, Hungary; GMH–Geiseltalmuseum, Martin
Luther University, Halle, Germany; HLMD–Hessisches Landesmuseum, Darmstadt, Ger-
many; IGM–Institute of Geology, Mongolian Academy of Sciences, Ulaan Baatar, Mongo-
lia; IRSNB–Institut royal des Sciences naturelles de Belgique, Brussels, Belgium; IVPP–
Institute of Vertebrate Paleontology and Paleoanthropology, Beijing, People’s Republic of
China; KNM–Kenya National Museum, Nairobi, Kenya; MACN–Museo Argentino de
Ciencias Naturales “Bernardino Rivadavia”, Buenos Aires, Argentina; MASP–Colección
del Museo de Ciencias Naturales y Antropológicas, Paraná, Argentina; MFN–Museum für
Naturkunde, Berlin, Germany; MGL–Geological Museum of Lausanne, Lausanne, Swit-
zerland; MGUH–palaeontology type collection, Geological Museum, University of Co-
penhagen, Copenhagen, Denmark; MHNT–Muséum de Toulouse, Toulouse, France;
MLP–Museo de La Plata, La Plata, Argentina; MNHN–Muséum National d’Histoire Na-
turelle, Paris, France; MPCN–Museo Patagónico de Ciencias Naturales, General Roca, Ar-
gentina; MPM–Museo Regional Provincal Padre Manuel Jesús Molina, Río Gallegos, Ar-
gentina; MUFYCA–Museo Florentino y Carlos Ameghino (Instituto de Fisiografía y Ge-
ología), Rosario, Argentina; MV – Musée Vivenel, Compiègne, France; NHMUK–Natural
History Museum, London, UK; NJSM–New Jersey State Museum, Trenton, New Jersey,
USA; NMNHS–National Museum of Natural History, Bulgarian Academy of Sciences,
Sofia, Bulgaria; NMNZ–Museum of New Zealand Te Papa Tongarewa, Wellington, New
Zealand; NNPM–National Museum of Natural History of the National Academy of Sci-
ences, Kyiv, Ukraine; ONU–Odes’kiy Natsional’niy Universitet, Odessa, Ukraine; PIN–
Palaeontological Institute, Russian Academy of Sciences, Moscow, Russian Federation;
PU–Princeton University Collection (now at Yale Peabody Museum), Princeton, New Jer-
sey, USA; QM–Queensland Museum, Brisbane, Australia; RAM–Raymond Alf Museum,
Claremont, California, USA; ROM–Royal Ontario Museum, Toronto, Ontario, Canada;
SAM–South Australian Museum, Adelaide, Australia; SGPIMH–Geologisch-Paläontolo-
gisches Institut und Museum der Universität Hamburg, Hamburg, Germany; UCMP–
University of California Museum of Paleontology, Berkeley, California, USA; UCR–Uni-
versity of California Riverside, Riverside, California, USA; UM–Museum of Paleontology,
University of Michigan, Ann Arbor, Michigan, USA; UNSW–University of New South
Wales; Sydney, Australia; USNM–Smithsonian Museum of Natural History, Washington
D. C., USA; WN–Michael C.S. Daniels collection, Essex, UK; YPM–Yale Peabody Museum,
New Haven, Connecticut, USA; ZIUU–Zoologiska Museum, Uppsala Universitet, Swe-
2. Overview of the Palaeognath Fossil Record
2.1. Lithornithidae
Lithornithids were small bodied, presumably volant birds that were first recognized
as palaeognaths by Houde and Olson [79], and described in detail as a clade by Houde
[62]. Thus far, they are only known from Europe and North America, contrasting with the
Gondwanan distribution of extant palaeognaths. At first glance, they appear remarkably
similar to tinamous, particularly in the shape of the skull. Fossil eggshells attributed to
lithornithids are also very reminiscent of those of tinamous, and it has been hypothesized
Diversity 2022, 14, 105 9 of 70
that lithornithids shared the same polygynandrous breeding behaviour of many extant
palaeognaths [62]. However, numerous characters distinguish tinamous and lithorn-
ithids, which are detailed by Houde [62]. On the basis of a more distally positioned del-
topectoral crest, longer and more curved humeral shaft, and a less distally elongated ster-
num in lithornithids compared with tinamous, Houde [62] also speculated that lithorn-
ithids were much more capable long-distance fliers than extant tinamous are. This idea
received further support from a reconstruction of the wing of a specimen of the Eocene
lithornithid Calciavis grandei with preserved carbonized feather traces, which indicated
that this species may have been capable of long-distance flapping flight [65].
Since their fossils are most often recovered from nearshore lacustrine or marine en-
vironments, it was suggested that lithornithids may have exhibited a shorebird-like ecol-
ogy [62], though this may be coincidental as these depositional settings are most likely to
produce fossils in general. The lithornithid jaw apparatus appears well suited to distal
rhynchokinesis, which allows a bird to capture food items in the ground without having
to fully open the jaws [62]. This suggests they could have used their bills for probing the
substrate for food items, in a manner more similar to kiwi than tinamous [62]. Additional
evidence for this type of foraging behaviour comes from the recognition of mechanore-
ceptors known as Herbst corpuscles in the rostrum of lithornithids [80], which form a tac-
tile bill-tip organ that picks up mechanical vibrations to detect buried prey.
A major unresolved question is whether Lithornithidae predate the K–Pg mass ex-
tinction. The cranial end of a right scapula with a distinctive pointed acromion was recov-
ered from the latest Maastrichtian or earliest Danian Hornerstown Formation in New Jer-
sey, USA [63]. If this material indeed belongs to a lithornithid, it would provide compel-
ling evidence that the clade survived across the boundary. However, it should be noted
that several Mesozoic stem ornithurines also have a hooked acromion that approaches the
condition seen in Lithornithidae [64,81,82]. Thus, the identity of this fossil remains uncer-
tain, and more material needs to be recovered from both this formation and other contem-
poraneous localities to clarify which groups of total-clade palaeognaths persisted across
the K–Pg boundary.
2.1.1. North American Lithornithids
Definitive lithornithid fossils are known from North America from the middle Paleo-
cene to the early Eocene (Figure 7, Table 1) [62,83–88]. The earliest uncontroversial record
on this continent is Lithornis celetius, from the middle Paleocene (early to middle Selan-
dian) Fort Union Formation of Montana and the Polecat Bench Formation of Wyoming
[62]. The entire skeleton of this species is known from a composite series of individuals
[62]. Slightly younger than L. celetius is a proximal end of a humerus from the middle
Paleocene (Tiffanian) Goler Formation in southern California. Despite being fragmentary,
its large, dorsally positioned humeral head and subcircular opening to the pneumotricip-
ital fossa diagnose it as a probable lithornithid, and it was assigned to the genus Lithornis
[88]. As nearly all North American lithornithids derive from the Rocky Mountain region,
this fossil extends their known range significantly further west.
Diversity 2022, 14, 105 10 of 70
Diversity 2022, 14, 105 11 of 70
Figure 7. Geographic distribution of palaeognath fossils illustrated on palaeogeographic globes. (top) Middle Paleocene, late Paleocene, early Eocene,
middle Eocene, late Eocene, and late Oligocene. (bottom) Early Miocene, middle Miocene, late Miocene, early Pliocene, and late Pliocene. Palaeomaps
modified from GPlates ( [83,84].
Diversity 2022, 14, 105 12 of 70
Table 1. Lithornithid fossil record.
Continent Geological Unit Location Epoch Stage Age Reference Taxa Institutions Reference
North America Hornerstown For-
mation New Jersey, USA Late Cretaceous–
early Paleocene
Olson and Parris [85];
Staron, et al. [86] ?Palaeognathae NJSM Parris and Hope [63]
Fort Union Formation Park County,
Montana, USA middle Paleocene Selandian Lofgren, et al. [87];
Stidham, et al. [88] Lithornis celetius USNM, PU Houde [62]
Polecat Bench For-
mation Wyoming, USA middle Paleocene Selandian Lofgren, et al. [87];
Stidham, et al. [88] Lithornis celetius PU, UM Houde [62]
Goler Formation
Kern County,
California, USA middle Paleocene Selandian
Lofgren, et al. [89];
Albright, et al. [90];
Lofgren, et al. [91]
Lithornis sp. RAM Stidham, et al. [88]
Willwood Formation,
Sand Coulee beds
Park County,
Wyoming, USA late Paleocene Thanetian Lofgren, et al. [87]
Lithornis promis-
Lithornis plebius
AMNH Houde [62]
Willwood Formation Basin, Wyoming,
USA early Eocene Ypresian Lofgren, et al. [87]
Lithornis nasi (pro-
visional), Paraca-
thartes howardae
UM, ROM, USNM Houde [62]
Green River For-
mation, Fossil Butte
Lincoln County,
Wyoming, USA early Eocene Ypresian Smith, et al. [92]
Calciavis grandei,
AMNH, USNM Houde [62]; Nesbitt
and Clarke [64]
Bridger Formation Bridger Basin,
Wyoming, USA middle Eocene Ypresian-Lutetian Murphey and
Evanoff [93] incertae sedis YPM Houde [62]
Europe Heers Formation, Orp
Sand member Maret, Belgium middle Paleocene Selandian Smith and Smith [94],
De Bast, et al. [95] cf. Lithornithidae IRSNB Mayr and Smith [96]
Fissure filling of Wal-
Helmstedt, Ger-
many middle Paleocene Selandian Aguilar, et al. [97] Fissuravis weigelti GMH Mayr [98]
Tuffeau de Saint-
France late Paleocene Thanetian
Steurbaut [99];
Moreau and Mathis
[100]; Smith and
Smith [94]
gen. et sp. indet. IRSNB Mayr and Smith [96]
Ølst Formation Limfjord region,
Denmark early Eocene Ypresian Heilmann-Clausen
and Schmitz [101]
Lithornis nasi,
Lithornis vultur-
MGUH Bourdon and Lindow
Fur Formation Denmark early Eocene Ypresian Chambers, et al. [103] Lithornis vultur-
inus DK, MGUH
Leonard, et al. [104];
Bourdon and Lindow
Diversity 2022, 14, 105 13 of 70
London Clay For-
Kent, Essex, Sus-
sex, England early Eocene Ypresian
King [105]; Ellison, et
al. [106]; Friedman, et
al. [107]
Lithornis vultur-
inus, Lithornis
nasi, ?Lithornis
hookeri, Pseudo-
crypturus cerca-
naxius (provi-
NHMUK, WN, PU Houde [62]
Messel Formation Messel, Germany middle Eocene Ypresian-Lutetian
Franzen and Hau-
bold [108]; Schaal
and Ziegler [109];
Lenz, et al. [110]
Lithornis sp. SGPIMH, IRSNB Mayr [111];
Mayr [112]
Diversity 2022, 14, 105 14 of 70
Two sympatric species are known from the late Paleocene (late Thanetian) Sand Cou-
lee Beds of the Willwood Formation in Wyoming. Lithornis promiscuus was the larger of
the two, and is the largest species in its genus [62]. Like L. celetius, virtually all bones of
the skeleton are known from a composite series [62]. The holotype, USNM 336535, pre-
serves the entire forelimb skeleton. The smaller Lithornis plebius is known from all major
appendicular elements [62]. Houde [62] acknowledged the possibility that L. promiscuus
and L. plebius may belong to a single sexually dimorphic species, but erred on the side of
a more conservative species diagnosis and retained them as separate taxa. Houde [62]
tentatively referred specimen NHMUK A 5303 from the London Clay on the Isle of Shep-
pey, UK to the latter species. Owing to both the homogeneity of the global hothouse cli-
mate and the shorter distance across the North Atlantic at the time, North American and
European avifaunas were remarkably similar during the late Paleocene and early Eocene
(e.g., [76,113,114]). Finding the same species on both sides of the Atlantic should therefore
not come as a surprise, and if NHMUK A 5303 is indeed an example of L. plebius it would
hint towards the dispersal capabilities of these birds.
The remaining North American lithornithids are Eocene in age. Paracathartes
howardae [115] was found in early Eocene strata of the Willwood Formation [62]. With the
exception of the sternum and pelvis, all bones of this species are again known from a com-
posite series [62]. The lacustrine Green River Formation deposited by the Gosiute, Uinta,
and Fossil palaeolakes in what is now Utah, Wyoming, and Colorado has yielded an enor-
mous wealth of fossils, most often preserved as slabs [116]. The Fossil Butte member of
the formation, deposited by the short-lived early Eocene Fossil Lake [116], has produced
the greatest number of lithornithid specimens thus far [64], as well as a great wealth of
other bird fossils (e.g. [117–128]). A minimum of two lithornithid species have been found
in this Lagerstätte [64]. The holotype of Pseudocrypturus cercanaxius [62] is a complete skull
and mandible, with nine cervical vertebrae in articulation [62]. A spectacular crushed ar-
ticulated specimen missing only the pelvis and caudal vertebrae is owned privately by
Siber and Siber, and a cast of this specimen is in the collections of the USNM. Two skele-
tons collected from the London Clay in England were provisionally referred to this species
[62], making it another lithornithid with a possible transatlantic distribution. The recently
named Calciavis grandei [64] was described from a complete, mediolaterally compressed
skeleton with preserved soft tissue including feathers, pedal scales, and claw sheaths. A
referred specimen includes most of the postcranial skeleton minus the femora and pelvic
region, and a disarticulated skull [64].
2.1.2. European Lithornithids
The fossil record of lithornithids in Europe also begins in the middle Paleocene, and
stretches to the middle Eocene (Figure 7, Table 1) [96,111,112]. The Orp Sand member
(early to middle Selandian) of the Heers Formation in Maret, Belgium yielded a distal
humerus fragment and a partial carpometacarpus that were assigned to Lithornithidae,
but the fossils are too incomplete to be assigned at a generic level [96]. The next oldest
European lithornithid, Fissuravis weigelti, is also known from fragmentary remains, in this
case the omal end of an isolated coracoid from the late middle Paleocene (Selandian) of
the fissure filling of Walbeck, Germany [98]. A lack of clear diagnostic features has cast
some level of doubt to this assignment. The coracoid lacks any lithornithid character other
than similarity in size, and seems to be missing the small foramina on the posteroventral
surface of the hooked acrocoracoid process that is an apomorphy of this clade [64]. Re-
gardless of the true affinities of Fissuravis weigelti, the Maret fossils demonstrate that
Lithornithidae stretch at least as far back in time in Europe as they do in North America.
As noted by Houde, one of the first fossil birds known to science was Lithornis vul-
turinus [62,129], the holotype specimen of which was purchased by the Royal College of
Surgeons in 1798. The holotype was sadly destroyed in the Second World War, though
detailed woodcut drawings of the holotype [130] allowed for the identification of a neo-
type by Houde [62]. The neotype, from the early Eocene (Ypresian) London Clay, was
Diversity 2022, 14, 105 15 of 70
originally identified as an early relative of turacos and named Promusophaga magnifica by
Harrison and Walker [131]. It consists of a right humerus, radius, ulna, and carpometa-
carpus, all missing the distal ends, a right scapula, partial sternum, distal left radius and
ulna, proximal left femur, proximal right tibiotarsus, a vertebral series, and ribs within a
clay nodule [62]. A large amount of fragmentary material from the London Clay, mainly
hindlimb elements, has been referred to this species [102]. A slightly younger specimen
from the early Eocene Fur Formation of Denmark preserves a three-dimensional skull in
articulation with a nearly complete postcranial skeleton and has been described in great
detail [102,104]. Another Danish fossil, a distal left humerus from the latest Paleocene-
earliest Eocene Olst Formation, was also referred to this taxon [102].
Lithornis nasi [132], also from the early Eocene London Clay Formation, was consid-
ered a junior synonym of L. vulturinus by Bourdon and Lindow [102]. As the material
comes from the type locality of L. vulturinus, these authors interpreted the differences be-
tween L. nasi and L. vulturinus as intraspecific variation. The holotype consists of proximal
fragments of a left humerus and right ulna, distal fragments of a right femur and a right
tibiotarsus, and two thoracic vertebrae [62]. Houde [62] tentatively assigned two speci-
mens from Early Eocene Willwood Formation to L. nasi. Another bird from the London
Clay, ?Lithornis hookeri [132], was tentatively referred to the genus by Houde [62]. The
holotype, a distal end of a tibiotarsus, suggests it was smaller than all currently known
lithornithids [62]. The Messel lithornithid from the middle Eocene of Germany (47–48
MYA) is the youngest lithornithid material yet discovered [111,112]. Known from a partial
postcranial skeleton and a skull that appear to represent the same species, it was assigned
to the genus Lithornis but not to a species-level taxon [112].
2.1.3. Systematics of Lithornithidae
While it is generally accepted that lithornithids are indeed total-clade palaeognaths,
important questions regarding their systematics remain: Do lithornithids represent a
monophyletic radiation of volant stem or crown palaeognaths? Do they represent a pa-
raphyletic grade of stem palaeognaths? Or, are they polyphyletic, with some taxa more
closely related to certain extant palaeognath lineages than others (Figure 8)? All three sce-
narios would seem to be possible considering that the earliest members of several extant
palaeognath subclades would most likely have been relatively small and volant. Houde
[62] argued that lithornithids are not monophyletic and placed Paracathartes closer to other
ratites on the basis of similar histological growth patterns, and the reduced, rounded post-
orbital process of its frontals. More recent authors have speculated that this histological
similarity exists because Paracathartes is larger than other lithornithids, reaching approxi-
mately the size of a turkey [76].
Diversity 2022, 14, 105 16 of 70
Figure 8. Possible relationships of Lithornithidae to the remainder of Palaeognathae. (a) Scenario A
shows a monophyletic Lithornithidae, (b) Scenario B shows a paraphyletic Lithornithidae, and (c)
Scenario C shows a polyphyletic Lithornithidae.
The phylogenetic analyses of both Nesbitt and Clarke [64] and Yonezawa, et al. [49]
recovered lithornithids as a monophyletic group. The character matrix used by Nesbitt
and Clarke [64] contained 182 characters combined from the morphological datasets of
Cracraft [5], Bledsoe [133], Lee, et al. [29], Mayr and Clarke [134], Clarke [81], Clarke, et
al. [135], and new observations gathered by the authors for 38 terminal taxa. In their un-
constrained analyses, Lithornithidae was recovered as the sister taxon to Tinamidae at the
base of Palaeognathae, congruent with previous morphological phylogenetic hypotheses.
This is unsurprising, given that lithornithids and tinamids share numerous skeletal simi-
larities that often optimize as synapomorphies of a lithornithid + tinamou clade. When
Paracathartes was constrained as sister to ratites, the resultant nonmonophyly of Lithorn-
ithidae added a significant number of steps to the analysis. The only character that sup-
ported this relationship was the reduction of the postorbital process of the frontal, which
the authors considered to be convergent. When relationships of living palaeognaths were
constrained to match those recovered by molecular phylogenies, lithornithids were recov-
ered as a clade of stem group palaeognaths. Though Nesbitt and Clarke [64] were unable
to achieve any resolution within Lithornithidae, lithornithid monophyly received rela-
tively high support. However, the authors acknowledge the need for future analyses as-
similating additional lithornithid character sets to further test the monophyly and phylo-
genetic position of lithornithids.
A strict consensus tree using parsimony constrained to match recent molecular phy-
logenetic topologies recovered a monophyletic Lithornithidae sister to Tinamidae, but
when the molecular constraint was removed and replaced with constraints enforcing sis-
ter group relationships between Palaeognathae + Neognathae and Neoaves + Gal-
loanserae, Lithornithidae instead resolved sister to a Dinornis + Dromaius + Struthio clade
to the exclusion of tinamous [136]. In an analysis of this same dataset with new characters
added and increased taxon sampling, Bayesian analysis placed lithornithids as stem pal-
aeognaths, and a maximum parsimony analysis of this dataset with cranial characters
weighted more strongly found strong support for a monophyletic Lithornithidae in this
same position [137]. When characters were unweighted in the maximum parsimony
Diversity 2022, 14, 105 17 of 70
analysis but constrained to a molecular backbone, a monophyletic Lithornithidae was
once again sister to Tinamidae [137]. Almeida, et al. [42] also recovered lithornithids as
sister to crown Palaeognathae in their Bayesian topology, but sister to tinamous in their
maximum parsimony and maximum likelihood trees. Maximum likelihood trees inferred
using characters exhibiting low homoplasy also supported a position on the palaeognath
stem for Lithornithidae [49], though the monophyly of the clade was dependent on the
matrix used. Ten non-homoplastic characters from Houde [62] yielded a paraphyletic
Lithornithidae, while 92 non-homoplastic characters from Worthy, et al. [136] supported
them as a monophyletic group. The authors considered their results as supportive of the
hypothesis that all extant palaeognaths evolved independently from Lithornis-like birds
[42]. Given lingering uncertainties regarding the monophyly and phylogenetic position of
lithornithids, a careful revaluation of character states and species limits within the group
would be timely, though this is beyond the scope of the present review.
2.2. African and Eurasian Palaeognaths: Struthioniformes
Two ostrich species are extant. The Common Ostrich Struthio camelus inhabits open
areas across much of sub-Saharan Africa, and the Somali Ostrich Struthio molybdophanes
of Eastern Africa was once considered conspecific with S. camelus but is now given species
status [17,138]. While the two extant species of ostrich are now confined to Africa, their
range extended into Asia during the Holocene. Ostriches may have persisted as far east
as Mongolia until 7,500 years ago based on Carbon-14 dating of eggshells [139] (though
see Khatsenovich, et al. [140] regarding uncertainties surrounding the dating of ostrich
eggs from Mongolia and Siberia), and ostriches of the subspecies S. c. syriacus, whose na-
tive range stretched from the Arabian Peninsula to Syria and Iraq, did not become extinct
until 1966 [17]. Ostriches are arguably the most cursorial of all birds, able to run at speeds
in excess of 70 km per hour [67]. Their extreme cursoriality is evinced by their unique foot
morphology: ostriches are the only extant didactyl birds, an anatomical configuration that
may be the result of similar selective pressures as those that drove digit reduction in
horses [77]. The fossil record of ostrich eggshell is rich, and although the present review
focuses only on skeletal remains, we note that the occurrence of palaeognath eggshells in
the early Miocene of China 17 million years ago [77,141] supports the theory that struthi-
onids either originated outside of Africa or else underwent rapid range expansion after
their emergence. For a thorough review of the ostrich eggshell record, see Mikhailov and
Zelenkov [78].
2.2.1. Eurasian Stem Struthionids
Our understanding of palaeognath evolution and particularly the transition to flight-
lessness in ratites has been hampered by a lack of recognizable stem group representatives
of extant palaeognath lineages. Fortunately, recent research advances have provided a
valuable window into the nature of early stem struthionids, which were previously un-
known prior to the Miocene. The flightless palaeognaths Palaeotis weigelti and Remiornis
heberti have long been known from the Paleogene of Europe [76,142–145], but their rela-
tion to the remainder of Palaeognathae was unclear [76,142]. Palaeotis, the better-known
of the two taxa, has been variably recovered as the sister taxon to rheids [146], sister to a
clade including Struthionidae, Rheidae, and Casuariidae [147], and sister to a clade com-
prised of lithornithids and tinamous [33]. The unconstrained analysis of Nesbitt and
Clarke [64] recovered Palaeotis outside a Struthio + Dromaius + Rhea clade. When relation-
ships of living palaeognaths were constrained to match those recovered by molecular phy-
logenies, the same authors recovered Palaeotis as the sister taxon of extant palaeognaths
(to the exclusion of lithornithids). Mayr [142] noted the resemblance of the skull of Palae-
otis to that of lithornithids, and that the scapulocoracoid differs from all extant ratites, but
was unable to find a well-supported placement for Palaeotis and proposed that it may rep-
resent yet another independent acquisition of ratite features among palaeognaths. The
phylogenetic position of Remiornis heberti was also challenging to estimate with
Diversity 2022, 14, 105 18 of 70
confidence. Mayr [76] considered that it may belong with Palaeotididae before amending
this hypothesis based upon the lack of a supratendinal bridge and extensor sulcus in Rem-
iornis, both of which are present in Palaeotis [148].
Without information on its palatal anatomy, it would be extremely difficult to recog-
nize Palaeotis as a palaeognath on the basis of its postcranial skeleton, as several aspects
of its hindlimb morphology, such as a notch in the distal rim of the medial condyle of the
tibiotarsus and intratendinous ossifications on the tarsometatarsus, are unusual for pal-
aeognaths and are more reminiscent of Gruiformes [148]. Recently, Mayr [148] transferred
Galligeranoides boriensis from the stem gruiform clade Geranoididae [149] to Palaeotididae.
G. boriensis had been described on the basis of leg bones from the early Eocene of France
[150]. Its initial assignment to Geranoididae was notable, as this clade was only known
from the Eocene of North America [76,149,151]. The transfer of G. boriensis from Gera-
noididae to Palaeotididae raises the possibility that additional records of early palaeog-
naths could be hiding in plain sight in museum collections, misidentified due to their lack
of obvious palaeognath synapomorphies.
This scenario was indeed the case with Eogruidae, a group of crane-sized birds
known primarily from hindlimb elements from Central Asia. Since the remainder of the
skeleton of eogruids was virtually unknown, these taxa were difficult to place phyloge-
netically. Eocene eogruids show a trend towards reduction in the size of the inner toe as
a possible adaptation for cursoriality [152], and later eogruids of the subclade Ergilornithi-
dae take this trend even further, to the point where the inner toe is vestigial or absent
[148,152]. This feature led several earlier authors to hypothesize a placement for Eogrui-
dae as stem struthionids [153–155]. However, this hypothesis was not widely accepted,
and eogruids were generally viewed as representatives of Gruiformes (either as sister to
a clade containing Aramidae and Gruidae [156] or sister to Gruidae [149]), implying that
the didactyly of some eogruids was convergent with Struthionidae.
A previously undescribed partial skull PIN 3110–170 from the latest Eocene locality
of Khoer Dzan, Mongolia has rendered the hypothesis of eogruids as gruiforms untenable
[6]. Although the palate is missing, the skull preserves an articular surface for the otic
capitulum of the quadrate, but apparently does not exhibit an articular surface for the
squamosal capitulum of the quadrate. Both articular surfaces would be expected for a
gruiform, and indeed for most neognaths, which have a bipartite otic process of the quad-
rate. Instead, the skull appears to genuinely exhibit only one articular facet for the quad-
rate, a condition seen only in palaeognaths [157]. This feature, in combination with the
reduction and eventual loss of the inner toe, strongly indicate a stem struthioniform place-
ment for Eogruidae. If taxa with greater toe reduction are more closely related to crown
struthionids, eogruids would form a paraphyletic grade along the ostrich stem lineage [6]
(Figure 9).
With the reassignment of Eogruidae, there is now a clear record of stem Struthionidae
in Eurasia well before the first crown struthionids appear in the Miocene of Africa. It now
appears likely that this iconic clade of extant African birds first arose outside the continent.
In addition to recognizing eogruids as stem struthionids, Mayr and Zelenkov [6] also hy-
pothesized that Palaeotis represents a total-clade struthionid based upon similarities in the
shape of its skull with the newly described specimen. With palaeotidids interpreted as
stem struthionids, the case for a Eurasian origin of Struthioniformes is strengthened even
further (Figure 9).
Diversity 2022, 14, 105 19 of 70
Figure 9. Relationships within Struthioniformes as hypothesized by Mayr and Zelenkov [6]. “Eogru-
idae” is here estimated to be a paraphyletic grade of crownward stem struthioniforms, and Gera-
noididae is tentatively inferred to be a clade of early stem struthioniforms.
The oldest flightless, non-lithornithid palaeognaths in Eurasia belong to Palaeotidi-
dae. Galligeranoides boriensis is now the oldest known probable palaeotidid, found in rocks
ranging between the ages of 56 to 51 Ma [158]. It is known from a right tibiotarsus, a distal
portion of a left tibiotarsus, and an incomplete right tarsometatarsus [150]. The nominate
and best known palaeotidid, Palaeotis weigelti, was initially interpreted as a bustard [145]
and subsequently as a crane [159] before it was finally recognized as a palaeognath by
Houde and Haubold [143], who hypothesized that it was as a stem ostrich despite its lack
of obvious cursorial adaptations, an assessment that, in light of the recent work discussed
above, has gained robust support. P. weigelti is known from six specimens from the middle
Eocene of the Messel and Geisel Valley sites of Germany (Table 2). One of these specimens
is a complete two-dimensionally preserved skeleton. It stood slightly under 1 meter tall,
and was more gracile than the older Remiornis [76].
Diversity 2022, 14, 105 20 of 70
Table 2. Fossil record of stem struthioniforms.
Continent Geological Unit Location Epoch Stage Age Reference Taxa Institutions Reference
Europe Châlons-sur-Vesles
Cernay and Berru,
Marne, France late Paleocene Thanetian Buffetaut and Angst
[160] Remiornis heberti MNHN
Lemoine [144];
Martin [161]; Mayr
Sables de Bracheux
Formation Rivecourt, France late Paleocene Thanetian Smith, et al. [162] Remiornis heberti MV Buffetaut and de
Ploëg [163]
Argiles rutilantes
d'Issel et de Saint-
Saint-Papoul, France early Eocene Ypresian Laurent, et al. [164];
Danilo, et al. [165] Galligeranoides boriensis MHNT Bourdon, et al. [150];
Mayr [148]
Messel Formation
Germany middle Eocene Ypresian-Lutetian
Franzen and Hau-
bold [108]; Schaal
and Ziegler [109];
Lenz, et al. [110]
Palaeotis weigelti HLMD
Peters [146]; Houde
and Haubold [143];
Mayr [142]
Geiseltal brown
Geisel Valley lignite
pits, Germany middle Eocene Lutetian Franzen and Hau-
bold [108] Palaeotis weigelti GMH
Lambrecht [145];
Houde and Haubold
[143]; Mayr [142];
Mayr [148]
Kolkotova Balka,
Tiraspol, Moldova late Miocene Tortonian-Mes-
Zelenkov and Kuro-
chkin [166] Urmiornis ukrainus PIN Zelenkov and Kuro-
chkin [166]
Hrebeniki, Odessa
Oblast, Ukraine late Miocene Tortonian-Mes-
Zelenkov and Kuro-
chkin [166] Urmiornis ukrainus NNPM Zelenkov and Kuro-
chkin [166]
Morozovka, Odessa
Oblast, Ukraine late Miocene Tortonian-Mes-
Zelenkov and Kuro-
chkin [166] Urmiornis ukrainus NNPM Zelenkov and Kuro-
chkin [166]
Armavir, Krasnodar
Krai, Russia late Miocene Tortonian-Mes-
Zelenkov and Kuro-
chkin [166] Urmiornis ukrainus Armavir Regional
Zelenkov and Kuro-
chkin [166]
unlisted Samos, Greece late Miocene Tortonian Zelenkov, et al. [167] Ampipelargus majori NHMUK Lydekker [168];
Zelenkov, et al. [167]
Triglia Formation
Kryopigi, Chalkidiki,
Greece late Miocene Tortonian-Mes-
Tsoukala and Bart-
siokas [169]; Laz-
aridis and Tsoukala
?Ampipelargus sp. AUG
Boev, et al. [171];
Zelenkov, et al. [167]
Asia Irdin Manha For-
Shara Murun region,
Inner Mongolia,
middle Eocene Lutetian Li [172] Eogrus aeola AMNH, PIN
Wetmore [173]; Ku-
rochkin [152]; Zelen-
kov and Kurochkin
Diversity 2022, 14, 105 21 of 70
Khaichin Formation
Omnogvi Province,
Mongolia middle Eocene Lutetian Zelenkov and Kuro-
chkin [166] Eogrus aeola PIN Zelenkov and Kuro-
chkin [166]
Obayla Formation
Kalmakpai River,
East Kazakstan late Eocene Priabonian Clarke, et al. [156] Eogrus turanicus PIN
Bendukidze [174];
Zelenkov and Kuro-
chkin [166]
Tsagan Khutel,
Bayanhongor Prov-
ince, Mongolia
late Eocene Priabonian Russell and Zhai
[175] Eogrus crudus PIN
Kurochkin [176];
Zelenkov and Kuro-
chkin [166]
Alag Tsav, Dornogovi
Province, Mongolia late Eocene Priabonian Dashzėvėg [177];
Clarke, et al. [156]
Eogruidae incertae
sedis IGM Clarke, et al. [156]
Kustovskaya For-
mation East Kazakstan late Eocene Priabonian Musser, et al. [178] Eogrus sp. PIN
Kozlova [179];
Kurochkin [176];
Musser, et al. [178]
Ergilin Dzo For-
Dornogovi Province,
latest Eocene-
earliest Oligo-
pelian Dashzėvėg [177]
Eogrus sp., Ergilornis
rapidus, Ergilornis mi-
nor, Ergilornis sp., Er-
gilornithidae incertae
sedis, Sonogrus gregalis
Wetmore [173]; Ko-
zlova [179]; Kuroch-
kin [152]; Kurochkin
[176]; Zelenkov and
Kurochkin [166];
Mayr and Zelenkov
Mynsualmas, Kazak-
stan early Miocene Aquitanian-Burdi-
Karhu [180]; Zelen-
kov and Kurochkin
Urmiornis brodkorbi PIN
Karhu [180]; Zelen-
kov and Kurochkin
Upper Aral For-
Altynshokysu, Kazak-
stan early Miocene Aquitanian-Burdi-
Karhu [180]; Zelen-
kov and Kurochkin
Urmiornis brodkorbi PIN
Karhu [180]; Zelen-
kov and Kurochkin
Tunggur Formation
Shara Murun region,
Inner Mongolia,
middle Miocene Serravallian Wang, et al. [181] Eogrus wetmorei AMNH [173]; Brodkorb
[182]; Cracraft [183]
Sharga, Govi-Altai
Province, Mongolia middle Miocene Serravallian Musser, et al. [178] Ergilornis sp.
Zelenkov, et al.
[167]; Musser, et al.
Nagri and Chinji
Gilgit-Baltistan, Paki-
late middle-
early late Mio-
nian Barry, et al. [184] ? Urmiornis cracrafti
Harrison and
Walker [185];
Musser, et al. [178]
unlisted Maragheh, Iran late Miocene Tortonian-Mes-
sinian Musser, et al. [178] Urmiornis maraghanus MNHN Mecquenem [186]
Diversity 2022, 14, 105 22 of 70
Lower Pavlodar
Formation Pavlodar, Kazakstan late Miocene Tortonian-Mes-
Zelenkov and Kuro-
chkin [166] Urmiornis sp. PIN
Kurochkin [176];
Zelenkov and Kuro-
chkin [166]
Karabulak For-
Kalmakpai, Zaisan,
East Kazakstan late Miocene Tortonian-Mes-
Zelenkov and Kuro-
chkin [166] Urmiornis orientalis PIN
Kurochkin [176];
Zelenkov and Kuro-
chkin [166]
Liushu Formation
Zhuangeji town,
Gansu, China late Miocene Messinian Fang, et al. [187] Sinoergilornis guanheen-
sis IVPP Musser, et al. [178]
Khirgis-Nur For-
Khirgis-Nur, Sunur
Province, Mongolia late Miocene Messinian Zelenkov and Kuro-
chkin [166] Urmiornis sp. PIN
Kurochkin [176];
Zelenkov and Kuro-
chkin [166]
Khirgis-Nur For-
Kobdos Province,
early Pliocene Zanclean Zelenkov and Kuro-
chkin [166]
Urmiornis dzabghanen-
sis PIN
Kurochkin [188];
Zelenkov and Kuro-
chkin [166]
Khirgis-Nur For-
Obo, Ubsunur Prov-
ince, Mongolia
early Pliocene Zanclean Zelenkov and Kuro-
chkin [166]
Urmiornis dzabghanen-
sis PIN
Kurochkin [188];
Zelenkov and Kuro-
chkin [166]
Diversity 2022, 14, 105 23 of 70
Eogruids are younger than Palaeotididae, occurring from the middle Eocene to the
early Pliocene, and comprise fifteen named species in six genera (Table 2). The oldest spe-
cies, Eogrus aeola, has been collected from the middle Eocene of Inner Mongolia and Mon-
golia’s Omnogvi Province [152,166,173] (Table 2). Like nearly all eogruids, it is known
only from hindlimb elements. Other members of this genus from the late Eocene include
Eogrus crudus from central Mongolia [176], and Eogrus turanicus from Eastern Kazakhstan
[174] (Table 2).
Outcrops of the latest Eocene-earliest Oligocene Ergilin Dzo Formation in Dorngovi
Province, Mongolia have produced an enormous wealth of eogruid fossils. It is in this
formation that Ergilornithidae first appear. Once recognized as a separate family [179],
they are now considered a subclade of Eogruidae [156,167]. Ergilornithids recovered from
this formation include Ergilornis rapidus [179], Ergilornis minor [176,179], and Sonogrus gre-
galis [176] (Table 2). The partial skull PIN 3110–170 was collected from the latest Eocene
Sevkhul member of this formation [6,155]. As the Sevkhul member has produced huge
quantities of hindlimb material belonging to Sonogrus gregalis and Ergilornis minor and no
other large birds, the skull was presumed to belong to one of the two species [6].
We were unable to find any documented occurrences of this clade for the remainder
of the Oligocene. The ergilornithid genus Urmiornis first appears in the early Miocene,
with two occurrences of Urmiornis brodkorbi in western Kazakhstan [180]. The latest occur-
rence of the genus Eogrus is in the middle Miocene of Inner Mongolia with Eogrus wetmorei
[173,182,183]. By the late Miocene, eogruids had expanded their range outside of Central
Asia and reached their greatest generic diversity, with Amphipelargus majori occurring on
Samos island [167,168] and another member of the same genus on the Greek mainland
[167,171], Urmiornis ukrainus occurring in Ukraine, Moldova, and southwestern Russia
[166,176], Urmiornis maraghanus in Iran [183,186,189], ?Urmiornis cracrafti in the Siwaliks
of northern Pakistan [185], and Sinoergilornis guangheensis in Gansu, China [178] (Table 2).
Although Kurochkin [176] noted differences between U. ukrainus and U. maraghanus, the
validity of U. ukrainus requires further conformation and U. maraghanus would take no-
menclatural priority if they are shown to be the same species [166]. The group continued
to thrive in their Central Asian stronghold, with Urmiornis orientalis found near Zaisan,
Kazakhstan [166,176] and Urmiornis sp. in the Sunur province of Mongolia and Pavlodar,
Kazakhstan [166,176]. The youngest species, Urmiornis dzabghanensis, was found in the
early Pliocene Khirgis-Nur Formation of Mongolia [166,188] (Table 2).
The possibility that the eogruids were flightless has been proposed by several authors
[152,173], though others contend that such a conclusion is premature based on existing
evidence [156,178]. The trochlea for the second toe is vestigial or entirely absent in Ergilor-
nis, Sinoergilornis, Urmiornis, and Ampipelargus [6,166,176,178], which is indicative of a
highly cursorial lifestyle as seen in extant struthionids. In addition, a proximal humerus
PIN 3110–60 from the Ergilin Dzo Formation attributed to Ergilornis has a greatly reduced
deltopectoral crest (the portion of the humerus serving as the major insertion point for
major flight muscles), and from this it was assumed that at least this taxon was flightless
[152]. If some eogruids were volant, it could imply that multiple transitions to flightless-
ness occurred among stem struthionids, following the phylogeny of Mayr and Zelenkov
(Figure 9) [6].
That the North American Geranoididae may also be struthioniforms has been sug-
gested on several occasions, but unlike Eogruidae no strong evidence for such a placement
has yet been found [6,148,155]. Geranoidids share several derived features with Palaeo-
tididae, including an elongated tarsometatarsus, a pronounced extensor sulcus along the
dorsal surface of the tarsometatarsus, a proximodistally elongated hypotarsus that forms
a long medial crest, and a notched distal rim of the medial condyle of the tibiotarsus [148].
With the recent reassignment of G. boriensis (discussed above), an investigation into pos-
sible palaeognath affinities for fossils assigned to the remaining members of this clade is
clearly merited. Eogeranoides campivagus from the Wilwood Formation of Wyoming has a
deep extensor sulcus along the dorsal surface of the tarsometatarsus, a feature it shares
Diversity 2022, 14, 105 24 of 70
with Palaeotis [142,148]. Considering that North American and European avifaunas were
generally similar during the Eocene [114,148], and that certain flightless bird taxa such as
Gastornithidae occurred on both sides of the Atlantic [76,77], the possibility that palaeo-
tidids existed in North America is plausible. A clade uniting Palaeotididae, Geranoididae,
Eogruidae, and Struthionidae is supported by the following characters highlighted by
Mayr and Zelenkov [6]: a very long and narrow tarsometatarsus, a short trochlea for digits
II and IV, a tubercle adjacent to the supratendinal bridge, and a shortening of all non-
ungual phalanges on pedal digit IV.
Also uncertain is the placement of Remiornis heberti [144] from the late Paleocene of
France [161] (Table 2). It is known from several isolated elements belonging to different
individuals that include a tibiotarsus, tarsometatarsus, and fragmentary associated re-
mains [76,161,163]. It appears to have been recognized as a palaeognath based on its over-
all resemblance to Palaeotis, as the two genera share a deep furrow on the dorsal surface
of the tarsometatarsus and a similar configuration of the distal trochleae [76]. Mayr [148]
excluded it from Palaeotididae based on its lack of an ossified supratendinal bridge and
extensor sulcus, and Mayr and Zelenkov did not include Remiornis at all in their new hy-
pothesis of struthioniform interrelationships [6]. However, in light of the variability ex-
hibited by the supratendinal bridge, extensor sulcus, and hypotarsus among palaeog-
naths, rejecting a struthioniform affinity for Remiornis may be premature. An ossified su-
pratendinal bridge of the tibiotarsus is present in Tinamidae and Dinornithidae and is
variably present in Apterygidae, but is missing from all other crown palaeognaths
[137,148]. Worthy et al. [137] note that given its variability in clades including crown Pal-
aeognathae and Cariamiformes, the presence or absence of this feature should not be
viewed to negate potential sister relationships. The extensor sulcus of the tibiotarsus is
also variably present in palaeognaths. It is narrow in Lithornithidae, Apterygidae, Tin-
amidae, and Dinornithidae, and absent in Struthionidae, Casuariidae, Rheidae, and Ae-
pyornithidae [148]. Eogruids have a hypotarsal canal, while all other palaeognaths lack
this feature [148]. The putative gruid Palaeogrus princeps [190] from the middle Eocene of
Italy also shares similarities in the distal tibiotarsus with Palaeotis and could represent yet
another record of this clade [148].
Several other taxa that deserve further revision of their taxonomic placement are
listed here, though it is far less likely that they belong within Palaeognathae. Eleutherornis
cotei [191,192] from the middle Eocene of Switzerland and France is known from a partial
pelvis and hindlimb elements and was originally assumed to be a ratite due to its large
size, but was reinterpreted as a phorusrhacoid [193]. Eremopezus eocaenus [194] is known
from hindlimb elements from the late Eocene Fayum Formation of Egypt [76,195]. Ras-
mussen, et al. [195] suggest that it could represent a non-palaeognathous endemic African
group that independently became large and flightless. More material will be needed to
firmly rule out palaeognathous affinities for this taxon [76]. Whether or not these species
are indeed palaeognaths, we expect that further revaluation of Paleogene fossil collections
is bound to reveal more palaeognaths from a critical time period that may capture their
transitions to flightlessness.
2.2.2. African and Eurasian Crown Struthionids
As shown in Table 3.
Diversity 2022, 14, 105 25 of 70
Table 3. Crown struthionid fossil record.
Continent Geological Unit Location Epoch Stage Age Reference Taxa Institutions Reference
Africa Elisabethfeld silts
Northern Sper-
rgebiet, Na-
early Miocene Aquitanian Pickford and Senut
[196] Struthio coppensi
Mourer-Chauviré, et al.
[197]; Mourer-Chauviré
unlisted Kadianga West,
Kenya middle Miocene Langhian Pickford [199] Struthio sp. KNM Leonard, et al. [200]
Nyanza, Kenya middle Miocene Serravallian Pickford [199] Struthio sp. KNM Leonard, et al. [200]
unlisted Ngorora, Kenya middle Miocene Serravallian Pickford [199] Struthio sp. KNM Leonard, et al. [200]
Beglia Formation
Bled el Dou-
arah, Tunisia late Miocene Tortonian Werdelin [201] Struthio sp. Rich [202]
Varswater For-
South Africa early Pliocene Zanclean Roberts, et al. [203] Struthio cf. asiaticus
Rich [204]; Manegold, et al.
[205], but see Mikhailov and
Zelenkov [78]
Ahl al
Oughlam, Casa-
blanca, Mo-
late Pliocene Piacenzian Geraads [206] Struthio asiaticus
Mourer-Chauviré and Ger-
aads [207], but see Mikhai-
lov and Zelenkov [78]
Olduvai series
Olduvai Gorge
Bed I, Tanzania early Pliestocene Gelasian Hay [208] Struthio oldawayi Lowe [209];
Leakey [210]
Aïn Boucherit,
Algeria early Pleistocene Gelasian Werdelin [201] Struthio barbarus Arambourg [211]; Mikhailov
and Zelenkov [78]
Asia Turgut strata Çandir, Turkey middle Miocene Langhian Becker-Platen, et al.
Struthio cf. brachydac-
tylus BGR Sauer [213]
unlisted Maragha, Iran late Miocene Tortonian Palaeostruthio karathe-
Mecquenem [189]; Lam-
brecht [214];
Mikhailov and Zelenkov
Baynunah For-
United Arab
Emirates late Miocene Tortonian Palaeostruthio karathe-
odoris Louchart, et al. [215]
Pavlodar, Ka-
zakhstan late Miocene Messinian (?) Palaeostruthio karathe-
Tugarinov [216]; Kurochkin
[188]; Mikhailov and Zelen-
kov [78]
Liushu Formation
Gansu prov-
ince, China late Miocene Tortonian-Mes-
sinian Deng, et al. [217] Struthio (Orientornis)
linxiaensis Hou, et al. [218]
Diversity 2022, 14, 105 26 of 70
Baode county,
China late Miocene Messinian Kaakinen, et al. [219] Struthio wimani Lowe [220]; Mikhailov and
Zelenkov [78]
Dhok Pathan For-
mation?, Siwalik se-
Siwalik Hills,
late Miocene-early
Sahni, et al. [221];
Sahni, et al. [222];
Stern, et al. [223]; Pat-
naik, et al. [224]
Struthio asiaticus
Davies [225];
Lydekker [226];
Mikhailov and Zelenkov
Çalta, Ankara,
Turkey early Pliocene Zanclean
Ginsburg, et al. [227];
Sen [228]; Janoo and
Sen [229]
Struthio sp. Janoo and Sen [229]
Pavlodar, Ka-
zakhstan early Pliocene Zanclean Struthio chersonensis Beliaeva [230]
upper Issykulian
Akterek, Kyr-
gyzstan late Pliocene Piacenzian Sotnikova, et al. [231] Pachystruthio trans-
caucasius Sotnikova, et al. [231]
Nihewan Formation
Nihewan Basin,
China early Pleistocene Gelasian Cai, et al. [232] Pachystruthio indet. MNHN Buffetaut and Angst [233]
middle-late Pleis-
Calabrian- Chi-
banian “Struthio anderssoni” Hou [234]
Europe unlisted Varnitsa, Mol-
dova late Miocene Tortonian Vangengeim and
Tesakov [235] Struthio orlovi Kurochkin and Lungu [236]
unlisted Pikermi, Greece late Miocene Tortonian Solounias, et al. [237] Palaeostruthio cf. kara-
theodoris Bachmayer and Zapfe [238];
Michailidis, et al. [239]
Nikiti Formation Nikiti, Greece late Miocene Tortonian Palaeostruthio cf. kara-
theodoris Koufos, et al. [240]
unlisted Hadzhidimovo,
Bulgaria late Miocene Tortonian Spassov [241] Palaeostruthio karathe-
odoris NMNHS Boev and Spassov [242]
late Miocene Tortonian- Mes-
Vangengeim and
Tesakov [235] Struthio novorossicus ONU Aleksejev [243]; Mikhailov
and Zelenkov [78]
unlisted Kuyal’nik,
Ukraine late Miocene Tortonian-Mes-
sinian Struthio sp.
Burchak-Abramovich [244];
Mikhailov and Zelenkov
unlisted Samos, Greece late Miocene Tortonian-Mes-
sinian Palaeostruthio karathe-
odoris MGL Forsyth Major [245]; Mikhai-
lov and Zelenkov [78]
Strumyani Genetic
Bulgaria late Miocene Tortonian- Mes-
Tzankov, et al. [246];
Spassov, et al. [247]
Palaeostruthio cf. kara-
theodoris NMNHS Boev and Spassov [242]
unlisted Kerassia,
Greece late Miocene Tortonian-Mes-
Theodorou, et al.
Palaeostruthio karathe-
odoris Kampouridis, et al. [249]
Diversity 2022, 14, 105 27 of 70
unlisted Grebeniki,
Ukraine late Miocene Tortonian Vangengeim and
Tesakov [235]
Palaeostruthio karathe-
odoris, Struthio brachy-
Burchak-Abramovich [250];
Mikhailov and Zelenkov
Odessa Catacombs Odessa,
Ukraine early Pliocene Zanclean Struthio sp. “Odessa
Ostrich” ONU
Burchak-Abramovich [244];
Mikhailov and Zelenkov
unlisted Kvabebi, Geor-
gia late Pliocene Piacenzian Pachystruthio trans-
Burchak-Abramovich and
Vekua [251]; Mikhailov and
Zelenkov [78]
Khapry Formation
Oblast, Russia
early Pleistocene Gelasian Tesakov [252]; Tesa-
kov, et al. [253]
Struthio sp. “Odessa
Ostrich” Kurochkin and Lungu [236]
Sésklo basin sedi-
mentary fill
Sésklo, Thes-
saly, Greece early Pleistocene Gelasian Struthio cf. chersonen-
sis Athanassiou [254]
unlisted Dmanisi, Geor-
gia early Pleistocene Gelasian Ferring, et al. [255] Pachystruthio dman-
Burchak-Abramovich and
Vekua [256]; Mikhailov and
Zelenkov [78]
Taurida Cave Taurida, Cri-
mea early Pleistocene Gelasian Lopatin, et al. [257] Pachystruthio dman-
isensis Lopatin, et al. [257]; Zelen-
kov, et al. [258]
unlisted Kisláng, Hun-
Pleistocene Gelasian-Calabrian Mayhew [259] Pachystruthio pannoni-
cus GMB Kretzoi [260]; Mikhailov and
Zelenkov [78]
Diversity 2022, 14, 105 28 of 70
The body fossil record of crown ostriches begins 21 million years ago in the early
Miocene of Africa with Struthio coppensi (Figure 7, Table 3), named on the basis of the shaft
and distal part of a left tibiotarsus, proximal left femur, distal left tarsometatarsus, right
tarsometatarsus shaft, and a left fibula from the early Miocene of the Northern Sperrge-
biet, Namibia [197]. As noted by Mourer-Chauviré [198], it was smaller and more gracile
than S. camelus, and a vestigial trochlea metatarsi II shows this early ostrich was didactyl
[197,198]. A late middle Miocene ostrich from western Kenya assigned to Struthio also had
a didactyl foot and was smaller than extant ostriches, though still larger than S. coppensi
[200]. Other Kenyan middle Miocene ostrich fossils have been discovered, but they remain
undescribed [78,261]. A distal tarsometatarsus was found from the middle-late Miocene
boundary in Tunisia [201,202], indicating their presence in North Africa. The size of this
bone is roughly comparable with that of the extant S. camelus [78].
No late Miocene ostrich body fossils have yet been found from sub-Saharan Africa,
but they are relatively common in Eurasia during this period (Figure 7, Table 3) [78]. A
pedal phalanx from the middle Miocene of Turkey is the oldest body fossil of crown stru-
thionids outside Africa [213]. From the late Miocene onwards, this clade occupied an enor-
mous geographical range, from the Balkans to northeastern China and eastern Siberia, and
south to India. The oldest ostrich from Eastern Europe, Struthio orlovi, was found in the
early late Miocene of Moldova [236]. Late Miocene Southern and Eastern European ostrich
species limits are somewhat contentious. S. karatheodoris [245] was larger than extant os-
triches [78], and many specimens from the Balkans have been referred to this taxon [238–
240,242,249]. A large pelvis from the late Miocene of the United Arab Emirates was as-
signed to this species based on its size [215], and sacral vertebrae of a very large ostrich
found in the terminal Miocene of northern Kazakhstan [188,216] may also belong to S.
karatheodoris [78]. S. novorossicus [243] is considered a nomem dubium by Mikhailov and
Zelenkov [78], as it cannot be distinguished from S. asiaticus. Koufos, et al. [240] suggested
that S. brachydactylus [250] may be a junior synonym of S. karatheodoris, but Mikhailov and
Zelenkov [78] consider them separate taxa, as S. brachydactylus was roughly the size of S.
camelus and therefore much smaller than S. karatheodoris. Mikhailov and Zelenkov [78]
refer Palaeostruthio sternatus [244] to S. karatheodoris, creating the new combination Pal-
aeostruthio karatheodoris.
Struthio (“Orientornis”) linxiaensis from the late Miocene of Gansu province, China is
one of the oldest East Asian ostriches [77,218,262]. Slightly larger than S. camelus, Mikhai-
lov and Zelenkov [78] argued that it likely belongs in its own genus, but tentatively treat
it as Struthio. Other late Miocene Asian ostriches include S. wimani, known from a frag-
mentary pelvis from China [220], and S. asiaticus [263] from the Siwalik series in North
India and Pakistan. The latter species has been treated as somewhat of a wastebasket
taxon, with eggshell fragments attributed to it from sediments as young as the late Pleis-
tocene of the Baikal region [264], and body fossils from as far away as South Africa
[204,205] (Table 3). Ostrich eggshells ranging in age from 11 to 1.3 Ma are known from the
Siwalik series [223]. However, the distribution, temporal range, and taxonomic identifica-
tions of these specimens are in need of revision.
Several large ostriches are known from the Pliocene. S. transcaucasius is known from
a pelvis from the late Pliocene of Georgia [251] and was recently assigned to the genus
Pachystruthio [258]. Many others have not been assigned to a species level taxon. It is evi-
dent from hindlimb fragments that a large ostrich existed in the lower Pliocene of South
Africa, which was referred to Struthio cf. asiaticus [204,205]. Pliocene fossils from Ahl al
Oughlam, Casablanca, Morocco, were also attributed to S. asiaticus [207]. Another large
ostrich is known from the early Pliocene of Central Turkey [229]. An ostrich from Odessa,
Ukraine, also from the early Pliocene, has only been assigned to Struthio [78,244].
Multiple species of large ostriches persisted through the Pleistocene. Struthio oldawayi
of the early Pleistocene of Tanzania was similar to the extant S. camelus, though consider-
ably larger [209,220]. Large Pleistocene ostrich bones from Kenya’s Olduvai Gorge site
may also belong to this species [210]. A large ostrich from the early Pleistocene of Algeria
Diversity 2022, 14, 105 29 of 70
was assigned to S. barbarus [201,211], and a middle Pleistocene cervical vertebra from the
Nefud desert in northeastern Saudi Arabia bears a close resemblance to the extant S. mo-
lybdophanes [265]. Two giant Eurasian ostriches of the early Pleistocene, Pachystruthio pan-
nonicus and Struthio dmanisensis, may be one species [258]. These birds were truly massive;
a femur from the lower Pleistocene Taurida Cave of Crimea yields a mass estimate of 450
kg [258] using the equation of Field, et al. [266]. A 1.8-million-year-old right femur from
Nihewan, North China may also belong to Pachystruthio. Assigned to Pachystruthio indet.,
its estimated mass is a smaller, though still enormous 300 kg [233]. S. anderssoni of the late
Pleistocene of eastern China [234] was 1.5 times the size of S. camelus, at about 270 kg
based on estimates from its minimum femur circumference [267]. Why ostriches disap-
peared across Eurasia remains a mystery. One hypothesis is that their decline was at least
partially linked to climatic cooling throughout the Cenozoic [77]. However, fossil egg-
shells indicating the possible persistence of ostriches in Mongolia well into the Holocene
[139] (though again, see Khatsenovich, et al. [140]) would seem to negate such an expla-
nation, and a stronger explanation for their disappearance is needed.
2.3. South American Palaeognaths: Rheiformes and Tinamiformes
South America is notable for being the only continent to host two family-level pal-
aeognath clades that have persisted to the present day. Two species belong to Rheidae,
the Greater Rhea Rhea americana and the Lesser Rhea or Darwin’s Rhea Rhea pennata (al-
ternatively Pterocnemia pennata in certain taxonomies). Both species are cursorial and in-
habit open areas, with the Greater Rhea’s range covering much of eastern and southern
South America while the Lesser Rhea is found in Patagonia and the Altiplano region
[68,268,269]. The Lesser Rhea was formerly placed in its own genus, Pterocnemia, but ge-
netic studies suggest it is closely related to the Greater Rhea, with which it can hybridize
[268,270]. There is some debate surrounding species limits among Lesser Rheas popula-
tions, as some consider the Altiplano subspecies R. p. garleppi and R. p. tarapacensis to form
a separate species from the nominate Patagonian subspecies, R. p. pennata [268].
Tinamous (Tinamidae) are by far the most speciose extant palaeognath clade, and
occupy a wide range of habitats in Central and South America [14]. The clade is divided
into two major subclades, the forest-adapted Tinaminae which contains 29 species in the
genera Tinamus, Crypturellus, and Nothocercus, and the open and arid habitat-dwelling No-
thurinae, with 17 species in the genera Taoniscus, Nothura, Nothoprocta, Rhynchotus, Eu-
dromia, and Tinamotis [14,42,271,272]. Like many ground-dwelling birds, tinamous have
short wings relative to their body size which results in high wing loading [273]. High wing
loading is associated with rapid flight but makes flight energetically costly [273], therefore
tinamous tend to escape from threats on foot unless flight is necessary [61]. The pectoral
muscles in tinamids are enormous relative to their body size, and allow for rapid takeoff
to escape potential predators [273,274].
2.3.1. Rheid Fossil Record
The oldest named ratite, Diogenornis fragilis, provides a key minimum-bound age es-
timate for the evolution of larger body size and flightlessness among palaeognaths. The
type specimen was found in the middle-late Paleocene of Itaboraí, Brazil and consists of
limb bones, vertebrae, and the tip of a premaxilla deriving from several individuals
[76,275]. The precise age of the Itaboraí fauna has been subject to debate, and an early
Eocene age has also been suggested [276]. However, the distal end of a right tibiotarsus
missing most of its lateral condyle from the even older middle Paleocene Rio Chico For-
mation of Argentina was also referred to this genus [277]. It was about two-thirds the size
of the Greater Rhea, and its wings were less reduced [77]. For biogeographical reasons,
Diogenornis is often presumed to be a stem rheiform [77,275]. However, Alvarenga [278]
reported casuariid affinities for Diogenornis, and [277] also noted dissimilarities between
the referred tibiotarsus and those of rheids. The cranial end of the medial condyle in me-
dial view is larger and projects further distally than the caudal portion, which optimizes
Diversity 2022, 14, 105 30 of 70
as a synapomorphy of casuariids [5,29]. While we consider it unlikely that Diogenornis
represents a casuariiform, the phylogenetic affinities of these fossils remain somewhat un-
certain. We conservatively treat D. fragilis as a total-clade rheid (Figure 7, Table 4). An-
other possible Paleogene rheid is represented by pedal phalanges from the middle Paleo-
cene of Patagonia [279].
Diversity 2022, 14, 105 31 of 70
Table 4. Rheid fossil record.
Continent Geological Unit Location Epoch Stage Age Reference Taxa Institutions Reference
South America Itaboraí Formation São José, Brazil late Paleocene Selandian Pascual and Ortiz-Jau-
reguizar [280] Diogenornis fragilis Alvarenga [275]
Rio Chico Formation Chubut province,
Argentina late Paleocene Thanetian Raigemborn, et al. [281] Diogenornis sp., Rheidae
indet. MACN Tambussi [279]; Agnolín
Koluel Kaike Formation El Gauchito, Chubut
province, Argentina late Paleocene Thanetian Krause and Bellosi
[282] gen. et sp. indet. MLP Agnolín [277]
Sarmiento Formation
Chubut province,
middle Eocene to
early Miocene unknown Paredes, et al. [283] gen. et sp. Indet. MACN Agnolín [277]
Chichinales Formation
Río Negro province,
Argentina early Miocene Burdigalian Kramarz, et al. [284] Opisthodactylus horaciope-
rezi MPCN Agnolín and Chafrat
Santa Cruz Formation Santa Cruz province,
Argentina early Miocene Burdigalian-
Marshall and Patterson
[286]; Fleagle, et al.
[287]; Blisniuk, et al.
[288]; Perkins, et al.
[289]; Cuitiño, et al.
Opisthodactylus patagonicus NHMUK, MPM,
Ameghino [291]; Buf-
fetaut [292]; Diederle and
Noriega [293]
Aisol Formation
Mendoza province,
Argentina early Miocene Burdigalian-
Langhian Forasiepi, et al. [294] Pterocnemia cf. mesopotam-
ica FMNH Agnolín and Noriega
Level 13 of Ganduglia
Río Negro province,
Argentina middle Miocene Langhian Ganduglia [296] gen et sp. indet. MLP Agnolín [277]
Ituzaingó Formation
Entre Ríos province,
Argentina late Miocene Messinian Cione, et al. [297]
Pterocnemia mesopotamica,
Pterocnemia sp., Rheidae
Agnolín and Noriega
Cerro Azul Formation La Pampa province,
Argentina late Miocene Messinian Cerdeño and Montalvo
[298]; Verzi, et al. [299] Pterocnemia sp. GHUNLP Cenizo, et al. [300]
Andalhuala Formation
Tucumán province,
late Miocene-early
Marshall and Patterson
[286]; Bossi and
Muruaga [301];
Reguero and Candela
Opisthodactylus kirchneri MUFYCA Noriega, et al. [303]
Monte Hermoso For-
Buenos Aires prov-
ince, Argentina early Pliocene Zanclean Deschamps, et al. [304];
Tomassini, et al. [305]
Heterorhea dabbenei, Hi-
nasuri nehuensis MLP Rovereto [306]; Tambussi
Diversity 2022, 14, 105 32 of 70
Other apparent ratite fossils from South America whose relations to modern palaeog-
naths are unclear are an incomplete right tibiotarsus from the middle Paleocene Koluel
Kaike Formation of Argentina [277], a pedal phalanx from a poorly dated portion of the
Sarmiento Formation that could be anywhere between middle Eocene and early Miocene
in age [283], and a distal end of a tibiotarsus from the late Miocene of Patagonia [277]. By
the late Miocene there was a marked increase in aridity across the continent, in contrast
with the paratropical and warm temperate forests that stretched all the way south into
Patagonia before this time [307]. Agnolín [277] puts forth the idea that this environmental
change could have led to the extinction of hypothetical forest-adapted non-rheid ratites in
South America, while favouring the open-habitat adapted rheids. Due to the high degree
of anatomical homoplasy among the various ratite lineages, we may never know the true
affinities of Diogenornis and these other unnamed ratite-like fossils with certainty, and can
only hope that further fossil material will be found that can shed light on their proper
phylogenetic placement and ecological habits.
Eocene bird records from South America are unfortunately rare in general [308]. The
next oldest rheid fossils are significantly younger, dating from the Miocene (Figure 7, Ta-
ble 4). Pterocnemia mesopotamica was found in the late Miocene of the Mesopotamia region
of Argentina [295], and an isolated tarsometatarsus referred to Pterocnemia cf. mesopotamica
could extend the temporal range of this species back to the middle Miocene [295]. Opis-
thodactylus kirchneri, another rheid from the late Miocene, was described on the basis of a
right femur, a right and left tibiotarsus, left and right tarsometatarsi, and pedal phalanges
[303]. The robust rheid Hinasuri nehuensis is known from a single left femur from the early
Pliocene of Buenos Aires province, Argentina [309]. Extant rheid species appear in the
Pleistocene, with Rhea anchorenensis [310] and Rhea pampeana [311] of the Pleistocene of
Argentina reassigned to the extant Greater Rhea (Rhea americana) [312,313].
2.3.2. Tinamid Fossil Record
The oldest fossils belonging to crown group Tinamidae appear in the early Miocene
Pinturas and Santa Cruz Formations of southern Patagonia (Figure 7, Table 5) [314–316].
This apparently abrupt appearance is most likely an artefact of the region’s limited Eocene
record. Molecular divergence time estimates suggest that the origin of crown Tinamidae
occurred in the late Eocene or early Oligocene, concurrent with large-scale cooling and
the emergence of open habitat in South America that led to turnover of the region’s mam-
malian fauna [42,317]. Most of these early Miocene fossils are fragmentary and cannot be
identified at a generic level, though phylogenetic analyses placed them within the open
habitat-specialised tinamid subclade Nothurinae [42,315]. A left humerus from the Santa
Cruz Formation was described as a new species, Crypturellus reai (Crypturellus is an extant
genus within the tinamid subclade Tinaminae, which is sister to Nothurinae [316]). Frag-
mentary remains from the late Miocene were assigned to the extant genera Eudromia and
Nothoprocta [300], both of which belong to Nothurinae. Only two species have been as-
signed to genera that are no longer extant: Roveretornis intermedius and Tinamisornis par-
vulus, both from the early Pliocene Monte Hermoso Formation [306,318], and Tinamisornis
was later referred to the extant genus Eudromia [319]. The extinct Eudromia olsoni was also
described from the same formation [320], and Nothura parvula was found alongside the
extant Nothura darwinii and Eudromia elegans in the late Pliocene Chapadmalal Formation
[308,321,322]. More recently, Nothura parvula was placed as sister to a Nothura + Taoniscus
+ Rynchotus + Nothoprocta clade [42]. As-yet undiscovered representatives of the Tin-
amidae stem group, which will likely be Eocene in age, are sorely needed to better under-
stand the evolutionary history of this group, and whether the ancestors of crown tinamids
were adapted for flight styles other than the highly specialized burst flight seen in tina-
mous today.
Diversity 2022, 14, 105 33 of 70
Table 5. Tinamid fossil record.
Continent Geological Unit Location Epoch Stage Age Reference Taxa Institutions Reference
South America Pinturas Formation Santa Cruz province,
Argentina early Miocene Burdigalian Fleagle, et al. [287] Tinamidae gen. et
sp. indet MACN Bertelli and
Chiappe [315]
Santa Cruz For-
Santa Cruz province,
Argentina early Miocene Burdigalian
Marshall and Patter-
son [286]; Fleagle, et
al. [287]; Blisniuk, et
al. [288]; Perkins, et
al. [289]; Cuitiño, et
al. [290]
Crypturellus reai,
Tinamidae gen. et
sp. indet
Bertelli and
Chiappe [315];
Chandler [316]
Cerro Azul For-
La Pampa province,
Argentina late Miocene Messinian
Cerdeño and Mon-
talvo [298]; Verzi, et
al. [299]
Eudromia sp., No-
thura sp. MLP, GHUNLP Cenizo, et al. [300]
Monte Hermoso
Buenos Aires prov-
ince, Argentina early Pliocene Zanclean
Deschamps, et al.
[304]; Tomassini, et
al. [305]
Eudromia olsoni,
Eudromia cf. ele-
ans, Roveretornis
intermedius, Tin-
amisornis parvulus
Brodkorb [318];
Tambussi and
Tonni [320]; To-
massini, et al. [305]
Chapadmalal For-
Buenos Aires prov-
ince, Argentina late Pliocene Zanclean-Piacen-
Marshall, et al. [323];
Deschamps, et al.
Eudromia elegans,
Eudromia sp., No-
thura parvula, No-
thura darwinii
Tambussi and Nor-
iega [324]; Tam-
ussi and Degrange
Diversity 2022, 14, 105 34 of 70
2.4. Australian Ratites: Casuariiformes
Both the cursorial emu and the graviportal cassowary belong to the family-level clade
Casuariidae [325]. The Emu Dromaius novaehollandiae is the only member of its genus, with
the recently extinct dwarf Kangaroo Island Emu D. baudinianus [326], King Island Emu D.
minor [327], and Tasmanian Emu D. diemenensis [328] now considered to be subspecies of
D. novaehollandiae [329–331]. Emu are found across most of continental Australia, with the
exception of areas of sandy desert and dense forest [332]. Cassowaries have an extremely
distinctive appearance, with a casque on the head and wattles on the neck. Unlike Emu,
cassowaries typically inhabit dense rainforest habitats. Three cassowary species are cur-
rently accepted: the Southern Cassowary Casuarius casuarius, the Dwarf Cassowary Casu-
arius bennetti, and the Northern Cassowary Casuarius unappendiculatus [66]. All three spe-
cies inhabit the island of New Guinea, and the Southern Cassowary’s range extends into
northeastern Queensland, Australia, and some adjacent islands. No casuariiform fossils
are known before the Late Oligocene [333], and thus far there is no indication that any
other palaeognath lineage has ever been present in Australia (Figure 7, Table 6).
Diversity 2022, 14, 105 35 of 70
Table 6. Casuarid fossil record.
Continent Geological Unit Location Epoch Stage Age Reference Taxa Institutions Reference
Australia Etadunna For-
Lake Palankarinna,
South Australia,
late Oligocene Chattian
Woodburne, et al.
[334]; Megirian, et
al. [335]
Emuarius guljaruba SAM Boles [333]
Wipajiri For-
Etadunna Station,
South Australia,
latest Oligocene-
early Miocene
Woodburne, et al.
[334]; Megirian, et
al. [335]
Emuarius gidju SAM, AM Patterson and Rich [336];
Boles [337]
Riversleigh fau-
nal zones A-C
Queensland, Aus-
latest Oligocene-
middle Miocene
Archer, et al. [338];
Travouillon, et al.
[339]; Megirian, et
al. [335]
Emuarius gidju AM, QM Boles [337]; Boles [340];
Worthy, et al. [341]
Camfield beds
Bullock Creek,
Northern Territory,
middle Miocene unknown Woodburne, et al.
[342] Dromaius sp.
Rich [343]; Rich and Van
Tets [344]
Waite Formation
Alcoota, Northern
Territory, Australia late Miocene unknown Rich [343] Dromaius sp. QM, UCMP
Woodburne [345]; Stirton,
et al. [346]; Rich [343];
Rich and Van Tets [344]
Chinchilla Sands
Chinchilla, Queens-
land, Australia early Pliocene Zanclean Rich and Van Tets
Dromaius novaehollan-
diae QM
Woods [347]; Stirton, et
al. [346]; Rich and Van
Tets [344]
Tirari Formation
Lake Palankarinna,
South Australia,
late Pliocene-early
Stirton, et al. [348];
Rich and Van Tets
Dromaius ocypus UCMP
Miller [349]; Rich [343];
Rich and Van Tets [344]
New Guinea Otibanda For-
Morobe, Papua
New Guinea late Pliocene Piacenzian Hoch and Holm
[350] Casuarius sp. UCMP
Plane [351]; Rich and Van
Tets [344]
Cave deposits unknown Pleistocene? Unknown Lydekker [168];
Miller [352] Casuarius lydekkeri AM
Lydekker [168]; Roth-
schild [353]; Miller [352];
Worthy, et al. [341]
swamp deposits
Pureni, Papua New
Guinea late Pleistocene Chibanian Williams, et al.
[354] Casuarius lydekkeri CPC Rich, et al. [355]
Diversity 2022, 14, 105 36 of 70
One of these early fossil Casuariiformes, Emuarius gidju [337], had a temporal range
spanning from approximately 24 Ma to 15 Ma and is known from a large number of spec-
imens [341]. E. gidju was first described on the basis of a distal tibiotarsus, proximal tar-
sometatarsus and shaft, and a complete pes from the Lake Ngapakaldi Leaf Locality of
the Wipajiri Formation in South Australia [336]. Two more specimens were found in late
Miocene deposits in Alcoota, Northern Territory [336,356], and even more from for-
mations spanning the late Oligocene to early late Miocene of Riversleigh, Queensland
[337,340]. The genus Emuarius differs from Dromaius in its retention of a cassowary like-
femur, while the tibiotarsus and tarsometatarsus have cursorial modifications and are
emu-like [337,340]. The pedal phalanges are of an intermediate morphology between the
extant emu and cassowary, being more dorsoventrally compressed than those of casso-
waries but less than those of emu [337,341]. This taxon is frequently used to calibrate mo-
lecular divergence dates between Casuarius and Dromaius, and a phylogenetic analysis of
morphological characters provided robust confirmation for E. gidju and Dromaius being
sister taxa [341]. The derived tibiotarsus and tarsometatarsus of Emuarius and Dromaius
likely evolved after the emu-cassowary split as the emu lineage began to evolve towards
a more cursorial mode of life [337,341]. The humerus is less reduced than in Dromaius,
which may represent the plesiomorphic state of a bird less removed in time from its volant
ancestors than extant Emu and cassowaries are [341]. E. gidju was smaller than the extant
D. novaehollandiae, with an estimated weight of 19–21 kg [340] compared with 30–55 kg in
emus [332]. Smaller orbits than Dromaius indicates Emuarius had smaller eyes relative to
its skull, and this feature combined with the limited extent of its cursorial specialisations
have been interpreted as being representative of the less open habitats present in Australia
before the continent underwent extensive aridification beginning in the latter half of the
Miocene [341,357].
Emuarius guljaruba, from the 24.1 Ma late Oligocene Etadunna Formation [333–336],
is known from a single complete left tarsometatarsus [333]. It is larger than E. gidju and
most likely a separate species, but its allocation to Emuarius remains provisional because
no femur has yet been discovered. The extant genus Dromaius first appears in the middle
Miocene Camfield beds of the Northern Territory [336,343]. Dromaius arleyekweke from the
late Miocene Waite Formation in the Alcoota scientific reserve, Northern Territory [358]
is the oldest named species in this genus. Small and gracile, it is notable in that it exhibits
extreme cursorial adaptation, with the tarsometatarsus even more elongated than in D.
novaehollandiae [358]. It was a small emu, with an estimated body mass based on tibiotar-
sus least shaft circumference using the algorithm of Campbell and Marcus [359] between
16 and 17.2 kg [358]. Derived features including a distally flattened external condyle of
the distal tibiotarsus, the elongated tarsometatarsus, a reduced trochlea metatarsi II as
compared with trochlea metatarsi IV, and a shallow median sulcus of the distal trochlea
metatarsi II indicate a close affinity with Dromaius rather than Emuarius [358]. The oldest
occurrence of the extant Dromaius novaehollandiae is in the early to middle Pliocene-aged
Chinchilla Sands of Queensland [336,346,347]. Another species, Dromaius ocypus, is known
from a tarsometatarsus from the Pliocene Tirari Formation of Lake Palankarinna, South
Australia [349]. D. arleyekweke was found as the sister taxon of D. ocypus and D. novae-
hollandiae [358]. With D. ocypus interpreted as less cursorial than either D. arleyekweke or
D. novaehollandiae, this relationship implies an independent acquisition of cursoriality in
D. arleyekweke or a loss in D. ocypus, which may complicate the traditional view of emu
evolutionary history as having involved a trend towards increasing cursorial specialisa-
tion [358].
The cassowary fossil record is very poor, likely owing to the clade’s preference for
tropical forest habitats in which fossils are unlikely to form or be found. Phalanges found
from the late Pliocene-aged Otibanda Formation of Papua New Guinea most closely
match the extant C. bennetti in size but do not appear similar enough to justify being con-
sidered conspecific [351]. Casuarius lydekkeri [353] is known from a distal right tibiotarsus
that is likely Pleistocene in age. The provenance of this fossil is debated [355], and may be
Diversity 2022, 14, 105 37 of 70
from Darling Downs, Queensland based on its preservation [331,341]. Worthy, et al. [341]
assessed the C. lydekkeri type material and concluded that its placement within Casuarius
is likely correct, but there are significant differences between it and the extant C. bennetti
and C. casuarius. A partial skeleton from swamp deposits dating to the late Pleistocene of
Pureni, Papua New Guinea was assigned to C. lydekkeri, and it was noted to be smaller
than any extant cassowary, with a more gracile femur [355]. Unfortunately, no elements
from this specimen overlap with those from the Otibanda Formation specimen [355], so
the relationship between the only known fossil cassowaries remains a mystery. Naish and
Perron [360] speculated that crown cassowaries may be a relatively young clade that
evolved in post-Pliocene Australia, with movement into New Guinea occurring during
the Pleistocene with the appearance of land bridges between the two landmasses. Of
course, this scenario will remain purely speculative until more of these elusive fossils
come to light.
2.5. New Zealand Ratites: Apterygiformes and Dinornithiformes
Until just a few centuries ago, New Zealand hosted two ratite lineages: Apterygi-
formes (kiwi) and Dinornithiformes (moa). Without mammalian competition, kiwi and
moa filled the niches of small terrestrial insectivorous and large browsing mammals re-
spectively. Five extant species of kiwi (Apterygidae) are currently recognized, all in the
same genus: the Southern Brown Kiwi Apteryx australis, the North Island Brown Kiwi Ap-
teryx mantelli, the Great Spotted Kiwi Apteryx haastii, the Little Spotted Kiwi Apteryx ow-
enii, and the Okarito Brown Kiwi Apteryx rowi [10]. Convergence between kiwi and small
ground mammals is often noted, and is indeed remarkable [361]: kiwi are relatively small-
bodied and nocturnal, with hair-like plumage and a superb sense of smell that compen-
sates for their poor vision. Their long bills are used to probe the soil and leaf litter for
invertebrates. Their eggs, which are the largest relative to body size of any bird, are laid
in burrows [10]. Additionally, they are unique in that they are the only known crown birds
with two functioning ovaries [362]. All five species face serious threats from introduced
mammalian predators, and introduction of kiwi to predator-free offshore islands has been
key to their continued survival [363]. Because of their sedentary nature, substantial local
diversity exists, and a study examining thousands of mtDNA loci found 16 to 17 genet-
ically distinct lineages within the five extant kiwi species [364].
Moa took the trend of forelimb reduction in flightless birds to the furthest possible
extreme by losing the forelimbs entirely. There is no indication of a humeral articular facet
on the scapulocoracoid, which itself is highly reduced and, along with the sternum, is the
only vestige of the pectoral girdle [77]. A vestigial furcula is present in the genus Dinornis
but is absent in all other moa [77]. Curiously, the forelimb-specific gene tbx5 that is essen-
tial for the induction of forelimb development appears to have been fully functional in
moa, suggesting that other developmental pathways were responsible for the loss of their
wings [365]. The moa clade exhibited an extreme degree of reverse sexual dimorphism
that for some time led to confusion regarding the number of known species-level taxa.
The accepted number of recent taxa based on ancient DNA is nine species in three families:
Dinornithidae, containing Dinornis robustus and Dinornis novaezealandiae, Megalaptery-
gidae containing the monotypic Megalapteryx didinus, and Emeidae, containing Anomalop-
teryx didiformis, Emeus crassus, Euryapteryx curtus, Pachyornis geranoides, Pachyornis elephan-
topus, and Pachyornis australis [11]. In the largest-bodied genus, Dinornis, females could be
up to three times larger than males, and it required a study of ancient sex-linked DNA
sequences to reveal that individuals of the previously recognized D. struthoides actually
represented the much smaller males of D. giganteus and D. novaezealandiae [366]. The ex-
tinction of moa is believed to have occurred extremely rapidly, within 200 years of human
settlement approximately 600 years BP [367]. Evidence of their existence remains in New
Zealand’s flora, some of which retains anachronistic defenses against browsing by moa
[368,369]. Moa coprolites and preserved gizzard contents indicate that they were
Diversity 2022, 14, 105 38 of 70
generalist herbivores, though some degree of species-specific dietary niche partitioning
existed [370].
How and when moa and kiwi arrived in New Zealand is still unknown [371], as un-
fortunately neither group has a clear fossil record from before the Pliocene [372]. Molecu-
lar phylogenetic evidence generally supports the hypothesis that moa and tinamous are
sister taxa [371], suggesting that moa and kiwi colonised New Zealand and became flight-
less independently. Depending on the timing of their arrival, both clades may have been
greatly affected by the Oligocene drowning of New Zealand, which culminated 25 Mya
[373,374]. Coincidentally, this time frame appears to have been a key interval for the emer-
gence of recognizable crown group representatives of other palaeognath clades on differ-
ent landmasses (Tables 3–6).
Debates regarding how much of Zealandia was above water during the Oligocene
drowning episode, and how this event impacted the origins of New Zealand’s endemic
flora and fauna continue [375,376]. Cooper and Cooper [377] postulate that only 18% of
the present land area was above sea level during peak inundation as a low-lying archipel-
ago. Trewick, et al. [376] and Landis, et al. [374] proposed that the islands were inundated
completely, meaning that the entirety of New Zealand’s terrestrial flora and fauna must
have arrived in the past 22 million years. An increasing amount of biological evidence
suggests at least some land must have remained above sea level during this period and
has shifted the consensus against a total inundation [372]. Divergence dating of taxa with
poor dispersal ability including frogs of the genus Leiopelma [378], Craterostigmus centi-
pedes [379], mite harvestmen [380], and zopherid beetles [381] indicates that taxa within
these groups diverged well before the drowning event, suggesting that all of them would
have needed to independently disperse to New Zealand post-flooding had it been fully
submerged. Wallis and Jorge [382] reviewed 248 published divergence dates between
New Zealand lineages and their closest relatives elsewhere and found evidence for 74
lineages that diverged before 23 Mya, and of those, 25 lineages dated back before Zea-
landia split from Australia, making them of true Gondwanan vicariant origin. Interest-
ingly, they found no evidence for a spike in extinctions or new arrivals around the time
of the transgression. No study has yet presented unequivocal geological evidence for com-
plete submergence [376,383], and clastic sediments deposited during the Waitakian stage
in the southern Taranaki Basin suggests a nearby terrestrial sediment source [384].
Cooper and Cooper [377] examined mitochondrial genetic diversity in kiwi, moa, and
acanthisitid wrens and found it to be unusually low compared to other ratites and other
avian taxa, and interpreted this as evidence for a bottleneck effect due to the Oligocene
drowning. They estimated that re-radiation of these endemic New Zealand lineages began
19–24 Mya. Could this be evidence that moa and kiwi survived the drowning in situ on
small islands, or that small volant founding populations arrived afterwards? The apparent
survival through the drowning event by other New Zealand taxa means the first scenario
is certainly possible. If absence of volant non-tinamid palaeognaths after the middle Eo-
cene is not an artifact of the fossil record, then the ancestral founding populations that
ultimately gave rise to kiwi and moa must have arrived before the drowning of New Zea-
land. Ultimately, only new fossil discoveries from before the drowning event are likely to
be able to resolve this question completely.
2.5.1. Apterygid Fossil Record
The oldest kiwi and moa fossils are from the St. Bathans terrestrial vertebrate faunal
assemblage from the early Miocene of St. Bathans, in the central Otago region of the South
Island (Figure 7, Table 7). The site is dated to 19–16 Ma [385,386], and has provided a rare
glimpse at New Zealand’s Neogene fauna just after the drowning of New Zealand. The
earliest known kiwi, Proapteryx micromeros, was described on the basis of a right femur
missing its distal condyles [387]. The only referred specimen is also fragmentary, consist-
ing of a left quadrate missing the orbital process anterior to the pterygoid condyle and
much of the lateral mandibular condyle [387]. Based on the femur circumference, the
Diversity 2022, 14, 105 39 of 70
estimated body mass of P. micromeros was between 234.1 and 377 g, making it only slightly
larger than the smallest extant kiwi, A. owenii [387]. If this species is representative of size
of the earliest total-clade apterygids, its size would seem to refute the hypothesis that kiwi
are phyletic dwarfs. The classic explanation for the extremely large eggs of kiwi was that
kiwi evolved from a large-bodied ancestor, and body size decreased over time while egg
size remained the same [361,388,389]. Instead, it may be more likely to have arisen as a
novel feature related to producing highly precocial young [387,390]. Based on the gracile
shape of the femur, the authors went as far as to propose that P. micromeros may have been
volant, though that hypothesis is impossible to assess on the basis of presently known
fossil material. If P. micromeros was volant, it would represent the only known example of
a volant stem member of an extant ratite lineage, and would indicate that kiwi may have
arrived in New Zealand after the drowning event. Recently, a 1-million-year-old kiwi fos-
sil from the North Island [391] was identified as a new species Apteryx littoralis [392]. No
other fossils of intermediate age are yet known between the St. Bathans fauna and the
Holocene, making it difficult to trace the origins of crown kiwi.
Diversity 2022, 14, 105 40 of 70
Table 7. Apterygid fossil record.
Continent Geological Unit Location Epoch Stage Age Reference Taxa Institutions Reference
New Zealand Bannockburn For-
Otago, South Is-
land, New Zealand
late early Mio-
cene Burdigalian
Mildenhall and Pocknall
[385]; Pole and Douglas
Proapteryx mi-
cromeros NMNZ Worthy, et al.
Kaimatira Pumice Marton, North Is-
land, New Zealand
middle Pleisto-
cene Calabrian Worthy [393] Apteryx littoralis NMNZ Tennyson and
Tomotani [392]
Diversity 2022, 14, 105 41 of 70
Thus far, the only molecular studies that sample multiple Apteryx species yield alter-
native estimates of the timescale over which species-level diversification within Apteryx
took place. Using concatenated sequences of nuclear and mitochondrial DNA, Grealy, et
al. [41] estimated that Apteryx mantelli diverged from other kiwi approximately 13 MYA,
whereas A. haastii and A. owenii diverged at about 4 MYA. The phylogenomic time tree
produced by Yonezawa, et al. [49] included nuclear and mitochondrial sequences from all
five extant kiwi species, and is in agreement with those divergence time estimates, infer-
ring an origin of crown group kiwi at approximately 12 MYA. By contrast, Weir, et al.
[364] inferred a much younger origin of the kiwi crown group at 3.85 MYA using mito-
chondrial DNA from a large sample of individuals. This was interpreted as evidence that
the kiwi radiation coincided with the last glacial period when populations were isolated
in glacial refugia, particularly those on the South Island [364].
2.5.2. Dinornithid Fossil Record
The St. Bathans fauna also provides a window into moa evolution (Figure 7, Table 8),
though the moa fossils known from this locality are even more fragmentary than those of
kiwi. Eggshell fragments found at the site suggest at least two species of moa were present
[372,394,395]. Several large avian bone fragments have been found, including one that was
identified as a portion of the proximal shaft of a right tibiotarsus [395]. Other large New
Zealand landbirds such as flightless adzebills and giant geese existed at the time, but the
fibular and outer cnemial crests are separated further on this tibiotarsus fragment than
they would be in those groups, and instead resemble those of palaeognaths most closely
[395]. One can only hope that the St. Bathans site yields bones that can be more conclu-
sively identified as belonging to early representatives of the moa lineage. Many late Pleis-
tocene-Holocene moa fossils are known [391,396], but Pliocene-Pleistocene moa fossils are
much scarcer, and very few are known from before the Otira glaciation event which began
~75,000 years ago [397]. A tibiotarsus assigned to Euryapteryx was found in marine mud-
stone reported to be Pliocene in age [397], and Dinornis was present on the North Island
at least two million years ago [397]. A tibiotarsus and tarsometatarsus fragments belong-
ing to Anomalopteryx didiformis were found in a clay bed below a basalt [398], and if they
are indeed older than the basalt and not fissure-fill, they would be about 2.5 million years
old [397].
Diversity 2022, 14, 105 42 of 70
Table 8. Dinornithid fossil record.
Continent Geological Unit Location Epoch Stage Age Reference Taxa Institutions Reference
New Zealand Bannockburn For-
Otago, South Is-
land, New Zea-
late early Miocene Burdigalian
Mildenhall and
Pocknall [385]; Pole
and Douglas [386]
Dinornithidae indet. NMNZ Tennyson, et al.
Timaru, South Is-
land, New Zea-
early Pleistocene Gelasian Mathews and Cur-
tis [399]
Anomalopteryx didi-
formis Forbes [398]; Wor-
thy, et al. [397]
Hawke’s Bay,
North Island,
New Zealand
early Pleistocene? Gelasian? Beu and Edwards
[400] Eurapteryx curtus AIM Worthy, et al. [397]
Wairapa, North
Island, New Zea-
early Pleistocene? Gelasian?
Oliver [401];
Beu and Edwards
“Eurapteryx geranoides” NMNZ Worthy, et al. [397]
Tewkesbury For-
Wanganui, North
Island, New Zea-
early Pleistocene Calabrian Beu and Edwards
Dinornis novaezealani-
dae, Emeidae indet. NMNZ Marshall [402];
Worthy, et al. [397]
Diversity 2022, 14, 105 43 of 70
As with kiwi, molecular time trees have yielded divergent hypotheses regarding the
timing of the moa radiation. Bunce, et al. [11] found evidence for the radiation being rela-
tively recent. The deepest divergence (between Megalapterygidae and the remaining fam-
ily-level moa taxa) was estimated at 5.8 MYA, within the same time frame as rapid moun-
tain formation on the South Island during the Miocene-Pliocene [11]. Indeed, the uplift of
the Southern Alps would have led to greater habitat diversity [403], and may have spurred
the diversification of moa. Interestingly, Haddrath and Baker [38] placed this earliest moa
divergence much earlier, at 19 MYA, which roughly coincides with the end of the Oligo-
cene drowning event. Regardless of when the earliest phylogenetic divergence within the
moa clade occurred, the fossil record suggests moa crossed onto the North Island via a
land bridge 1.5–2 million years ago, which may have led to even greater species diversity
as the land bridge reappeared and disappeared during Pleistocene glacial cycles [11].
Whether kiwi were similarly restricted to the South Island before the Pleistocene is un-
known, and more fossils from sediments of intermediate age between the Miocene and
Pleistocene are needed to make any further advances.
2.6. Malagasy Ratites: Aepyornithiformes
Extremely little is known of the evolutionary history of Madagascar’s giant elephant
birds. The island’s Cenozoic terrestrial vertebrate record is notoriously poor, and thus far
all fossil finds are restricted to the last 80,000 years [404–406]. What little we do know
comes from subfossil bones and eggshells, the latter of which are extremely abundant in
some areas. Detailed records of late Pleistocene and Holocene aepyornithid subfossils are
beyond the scope of this paper, but can be found in Angst and Buffetaut [407]. Isotopic
analysis of eggshells from southern Madagascar reveals that the birds that laid them
mainly browsed on non-succulent trees and shrubs [408], some of which retain anachro-
nistic defenses against ratite browsing similar to plants in New Zealand [369]. Palaeoneu-
rological evidence shows that elephant birds had extremely reduced optic lobes, presum-
ably associated with a predominantly nocturnal or crepuscular lifestyle [409].
Even the number of elephant bird species that existed into the Holocene is not known
with certainty. Morphometric analysis of subfossil limb bones by Hansford and Turvey
[12] recovered evidence for four species-level taxa: Mullerornis modestus, Aepyornis hilde-
brandti, Aepyornis maximus, and the heaviest bird ever discovered, Vorombe titan. M. mod-
estus, A. maximus, and V. titan were found to be sympatrically distributed across much of
Madagascar, while A. hildebrandti was restricted to the central highlands [12]. Molecular
studies are needed to evaluate this morphology-based taxonomic scheme, as well as ad-
ditional fossil collecting in other regions of Madagascar, as most known specimens come
from the south of the island and the central highlands [12]. Nuclear and mitochondrial
DNA recovered from eggshells suggested that Aepyornis and Mullerornis diverged ap-
proximately 27.6 MYA [41]. A divergence at 3.3 MYA between A. hildebrandti and A. max-
imus had previously been estimated [45]. The third genus found by Hansford and Turvey
[12] appears not to have been sampled, highlighting the need to extract aDNA from addi-
tional eggshells and subfossil specimens.
Unraveling the decline and eventual demise of elephant birds in Madagascar is less
straightforward than for moa, which went extinct within a brief window of time following
human arrival in New Zealand [367]. Debate as to how long humans have been present
on Madagascar, and thus for how long they coexisted with the island’s endemic mega-
fauna, is ongoing. Based on rare findings of stone tools and butcher marks on elephant
bird bones, humans may have arrived early, between 10,000 and 4000 years BP [410,411].
Some anthropologists advocate a more recent arrival, between 1600 and 1000 BP [412],
while an intermediate arrival time between 2000 and 1600 BP is supported by 14C data
associated with human activity [413]. If humans and elephant birds indeed coexisted for
a long period of time, their extinction cannot be easily attributed to the rapid overkill of a
naïve population as with moa [411,414]. Instead, a more complex scenario for the extinc-
tion of the Malagasy megaherbivores, which also included giant lemurs and tortoises, as
Diversity 2022, 14, 105 44 of 70
well as dwarf hippopotami, has been proposed. Instead of overhunting, the key factor in
their decline may have been the introduction of livestock such as Zebu cattle and a shift
towards pastoralism. The introduction of large herbivores by humans coincides with the
time frame of Malagasy megafaunal extinction, and under this scenario a combination of
resource competition with introduced herbivores, alteration of the landscape by humans
to suit the needs of livestock, and increased bushmeat hunting due to the expanding hu-
man population could have led to the demise of the Malagasy megafauna [414]. Whatever
the direct cause or causes, the extinction of Aepyornithidae occurred roughly 1,000 years
BP according to radiometric data [415], concurrent with the drastic decline and extinction
of the remainder of the endemic megafauna of the island [416], though some colonial rec-
ords suggest they may have survived in isolated areas into the 17th century [407,417].
2.7. Antarctic Ratites
Antarctica was once a very different place from the frozen continent we recognize
today. The formation of a continental ice sheet did not occur until the Eocene—Oligocene
boundary [418]. Up until this time, the continent boasted thriving flora and fauna that
were isolated from large mammalian predators—an ideal environment for flightless birds
to evolve. Palynological records from sediment cores dated to 53.6–51.9 MYA from the
eastern Antarctic Wilkes Land coast reveal that a diverse paratropical rainforest with
frost-free winters existed during the early Eocene climatic optimum [419,420]. Sparse pol-
len from more cold-tolerant trees such as Nothofagus (southern beech) and Araucaria
(“monkey puzzle”) trees suggest temperate rainforests further inland [419,420]. By the
middle Eocene, cores from 49.3–46 MYA indicate species diversity had decreased [420]
and that cool temperate Nothofagus-dominated forests had taken over [419,420]. As a point
of comparison, petrified wood samples from King George island in the South Shetland
Islands aged 49–43 MYA (Middle Eocene) indicate a forest similar in composition to the
cold temperate Valdivian rainforest of Chile [421], which is not dissimilar to the temperate
rain forests of New Zealand that moa once inhabited.
There is fossil evidence of large terrestrial birds in Antarctica during this time, but
they are too fragmentary to allow firm diagnoses (Table 9). A distal fragment of a right
tarsometatarsus purported to be a ratite was found in the middle Eocene of the La Meseta
Formation of Seymour Island, just off the Antarctic peninsula [422]. Unfortunately, there
is no evidence for its ratite affinities other than its large size. Its unusually large trochlea
for the second toe is different from that of all other known ratites [76], and it bears consid-
eration that misattribution of large bones to ratites is not uncommon [423]. An anterior
part of a premaxilla originally attributed to a phorusrhacid, also from the La Meseta For-
mation [424–428], was recently suggested to belong to a palaeognath [429,430]. The pres-
ence of ratites on Seymour Island would not be surprising given the environmental con-
ditions at the time, as evidenced by abundant petrified conifer wood from the La Meseta
Formation [431]. Confirmation of their existence will have to await more complete speci-
mens, but remains a tantalizing possibility.
Diversity 2022, 14, 105 45 of 70
Table 9. Putative Antarctic ratites.
Continent Geological Unit Location Epoch Stage Age Reference Taxa Institutions Reference
Antarctica La Meseta For-
mation Seymour Island late Eocene Lutetian-Pria-
bonian Amenábar, et al. [432] “ratititae” MLP, UCR
Tambussi, et al.
[422]; Cenizo [429];
Acosta Hospitaleche,
et al. [430]
Diversity 2022, 14, 105 46 of 70
The majority of Cenozoic Antarctic bird fossils belong to penguins and other marine
birds, but Seymour Island was also host to a thriving terrestrial fauna during the Eocene.
The stem falconid Antarctoboenus carlinii [433,434] was named from a distal end of tarso-
metatarsus from the early Eocene portion of the La Meseta Formation [430]. Small mam-
mals were abundant, and included the extinct and highly enigmatic sudamericid gond-
wanatheres [435,436] as well as didelphimorphid, polydolopimorphid, and microbiothe-
riid marsupials [436–440]. Seymour Island also hosted South American meridiungulates
[436,441–445], and a large sparnotheriodont with an estimated body mass of 395–440 kg
[446] indicates the ecosystem was fully capable of sustaining large herbivores. The pres-
ence of meridiungulates also indicates that overland dispersal from South America was
possible, and there is no reason why South American ratites could not have made the
journey as well. The Drake passage between South America and the Antarctic Peninsula
did not begin to open until approximately 41 Ma [447], meaning these faunas lived during
an era where biotic interchange was possible. Such interchange with Australia was also
hypothetically possible for a brief window during the Paleocene and early Eocene, as di-
nocyst assemblages indicate the flow of ocean water across the Tasman gateway by 50–49
Ma [448]. It is also possible for a unique ratite lineage to have arisen on Antarctica,
though—as with all other ideas regarding Antarctic palaeognaths—this will remain
highly speculative until more fossils are recovered. Regardless of whether the Antarctic
terrestrial fauna included ratites, the complete glaciation of the continent in the Oligocene
would have doomed them to extinction.
3. Molecular Phylogenetic Hypotheses of Palaeognath Interrelationships
Interpreting phylogenetic relationships among extant and fossil palaeognaths was
historically challenging due to morphological homoplasy, and although molecular phy-
logenetic approaches have yielded some consensus on palaeognath interrelationships, ar-
eas of disagreement remain. Thus far, all recent molecular phylogenetic studies of pal-
aeognaths have recovered ostriches as the sister taxon to the rest of the clade, yielding
congruent support for a reciprocally monophyletic clade called Notopalaeognathae com-
prising rheas, tinamous, kiwi, moa, and elephant birds [36–41,44–46,48–50,54–58,449,450].
Limited morphological evidence has also been found in support of a monophyletic Noto-
palaeognathae [33,77]. In addition, all molecular phylogenetic studies investigating an-
cient DNA from palaeognath subfossils have strongly supported elephant birds as sister
to kiwi [41,45,46,49,57], and tinamous as sister to moa [38,40,41,44–46,49,50,57].
The internal relationships of Notopalaeognathae remain controversial, particularly
in regard to the position of rheids. The internal branches at the base of Notopalaeognathae
appear to be very short, indicating that the clade may have undergone relatively rapid
diversification early in its history, which may have led to incomplete lineage sorting and
limited phylogenetically informative character acquisition along deep internodes
[38,39,56]. This may have pushed Notopalaeognathae into an empirical anomaly zone in
which the most common gene trees from molecular phylogenetic analyses do not match
the species tree [56]. Rheids are most often recovered in one of two phylogenetic positions:
1. As the sister taxon of the remaining notopalaeognaths [36,37,39,41,42,44–
46,48,49,54–56], though this position is generally weakly supported (Figure 10) [41,44,49].
2. As sister to a casuariid + apterygid + aepyornithid clade (“Novaeratitae”)
[38,43,48,50,56–58,450] (Figure 11). Several alternative topologies in addition to these have
been recovered that place rheas sister to the tinamid-dinornithid clade [37,39,449] or sister
to casuariids [38].
Diversity 2022, 14, 105 47 of 70
Figure 10. A summary of recent molecular phylogenetic studies that recover Rheidae as sister to the
remaining notopalaeognaths. Extinct clades are indicated by †. (a) Smith, et al. [39] primary con-
cordance and total evidence tree. (b) Prum, et al. [48] concatenated dataset; Kuhl, et al. [54]. (c)
Hackett, et al. [36]; Harshman, et al. [37] maximum likelihood and Bayesian tree; Claramunt and
Cracraft [55]. (d) Phillips, et al. [44]; Cloutier, et al. [56] concatenated dataset. (e) Mitchell, et al. [45];
Grealy, et al. [41]; Yonezawa, et al. [49], Urantówka, et al. [46], Almeida, et al. [42].
Diversity 2022, 14, 105 48 of 70
Figure 11. A summary of recent molecular phylogenetic studies that do not recover Rheidae as sister
to the remaining notopalaeognaths. Extinct clades are indicated by †. (a) Kimball, et al. [450]. (b)
Prum, et al. [48] binned ASTRAL analysis; Reddy, et al. [58]; Sackton, et al. [50]; Feng, et al. [43]
maximum likelihood analysis of avian growth hormone gene copies. (c) Haddrath and Baker [38]
10 and 27 gene concatenated dataset, 27 gene consensus tree; Baker, et al. [40]; Cloutier, et al. [56]
total evidence consensus tree. (d) Haddrath and Baker [38] 10 gene consensus tree. (e) Smith, et al.
[39] maximum likelihood reanalysis of Phillips, et al. [44]; (f) Harshman, et al. [37] maximum parsi-
mony and RY coded maximum likelihood analysis; Wang, et al. [449]; (g) Smith, et al. [39] using 40
Determining why these discrepancies exist could be key to finally resolving the in-
ternal branching order of Notopalaeognathae. In their attempt to address this question
using genome-wide datasets of conserved nonexonic elements, introns, and ultracon-
served elements, Cloutier, et al. [56] found that the consensus species tree building meth-
ods MP-EST and ASTRAL-II placed rheids sister to the casuariid-apterygid-aepyornithid
clade with maximal bootstrap support from MP-EST for all three datasets. Their
Diversity 2022, 14, 105 49 of 70
concatenated supermatrix dataset recovered rheids as sister to all other notopalaeognaths,
but with weaker statistical support. In general, concatenated analyses have often yielded
different results to consensus tree building methods regarding the interrelationships of
Notopalaeognathae, with concatenated data more frequently recovering rheids as sister
to all other notopalaeognaths [56]. Sackton, et al. [50] found similar results and claim that
their genome-wide approach is more robust to incomplete lineage sorting than concate-
nation, which is what leads to discrepancies between studies. “Novaeratitae”, a proposed
clade that places casuariids sister to an elephant bird + kiwi clade, received high bootstrap
support when mitochondrial and genomic data were combined but not when each were
analysed individually [41]. In order to finally resolve the messy internal relationships of
notopalaeognaths, a greater number of faster-evolving retrotransposons and introns may
need to be analysed [41], and the models of sequence evolution employed must fit the
type of genomic data being investigated [58].
Molecular Divergence Time Estimates
The vast majority of molecular divergence time analyses have recovered an estimate
for the palaeognath-neognath divergence in the Cretaceous Period, preceding the K–Pg
extinction event (e.g. [38,41,42,44,45,47–49,54,55,449]), an estimate that is consistent with
the known (yet sparse) fossil record of Mesozoic neornithines [72]. However, estimates of
the age of the neornithine root vary enormously, ranging from 131 Ma [38] to 63.2 Ma [42].
Importantly, the oldest published divergence time estimates do not invalidate Gond-
wanan vicariance as a potential driver of crown palaeognath divergences [38]. The enor-
mous temporal breadth of deep neornithine divergence time estimates have stimulated
discussion about the role of model misspecification in driving erroneously ancient diver-
gence time estimates [451]. Hypothesized selection for reduced body size across the end-
Cretaceous mass extinction event could have transiently increased molecular substitution
rates along the deepest branches within neornithine phylogeny, which would be expected
to drive overestimates of node ages around the neornithine root [452]. Indeed, simulations
suggest that 40 million years’ worth of age disparity for the neornithine root node can
plausibly be explained by the effect of body size on nucleotide substitution rates [452].
Importantly, the palaeognath stem lineage is inferred to have exhibited high nucleotide
substitution rates, consistent with ancestral palaeognaths having been small-bodied (the
last common ancestor of crown palaeognaths was estimated to have weighed approxi-
mately 2.9 kg) [452]. With smaller body sizes and shorter generation times than other ex-
tant palaeognaths, tinamous exhibit anomalously high nucleotide substitution rates com-
pared with other palaeognaths [37,449], which may additionally drive erroneously ancient
divergence time estimates near the neornithine root [45,453].
Lingering uncertainty regarding the phylogenetic divergence times of crown pal-
aeognaths complicates attempts to place lithornithids within the broader context of pal-
aeognath evolution. Since most palaeognath divergence time estimates pre-date the earli-
est well corroborated lithornithid fossils [41,45,49,449] (with the possible exception of the
~66 million year old isolated scapula from the Hornerstown Formation [63]), the hypoth-
esis that at least some lithornithids represent early stem group representatives of major
palaeognath subclades is temporally viable. However, Prum, et al. [48] estimated the
origin of the palaeognath crown group at 51 Ma, during the Ypresian stage of the early
Eocene. In this temporal scenario, most lithornithid fossils predate the crown palaeognath
radiation, in which case nearly all lithornithids with the exception of those found in the
younger Messel Formation could only represent stem palaeognaths. This relatively young
age for the palaeognath crown group would also imply that early Paleogene remains such
as Diogenornis, Palaeotididae, and the Middle Paleocene fossils identified as belonging to
a stem rheid fall outside the palaeognath crown group.
Diversity 2022, 14, 105 50 of 70
4. Key Gaps in the Palaeognath Fossil Record
4.1. Cretaceous Stem Palaeognaths
Virtually no examples of Cretaceous stem palaeognaths have yet been identified, de-
spite consensus—on the basis of divergence time estimates as well as the presence of fossil
total-clade neognaths—that they must have existed at this time. This is perhaps the most
glaring gap in the known palaeognath fossil record, but is perhaps an unsurprising one
given the general scarcity of well-supported Cretaceous neornithines at present. A prob-
able example of a Cretaceous total-clade neognath is Vegavis iaai, recovered from the late
Maastrictian of Vega Island, Antarctica [69]. This fossil taxon shows apparent specialisa-
tions for foot-propelled diving, and has been variably placed within Anatoidea [69], as a
stem neognath, or even outside of Neornithes altogether [72,454]. Asteriornis maastrichten-
sis, from the Maastrichtian of Belgium, is another probable Cretaceous total-clade ne-
ognath. At 66.7–66.8 million years old, Asteriornis is slightly older than Vegavis, and there-
fore the oldest well-corroborated neornithine yet discovered [72]. A relatively small bird
(estimated to have weighed roughly 490 grams), Asteriornis was identified as a total-clade
galloanseran [72], although a recent study raised the (weakly supported) hypothesis that
it instead represents a total-clade palaeognath [8]. The presence of probable total-clade
neognaths from before the K-Pg mass extinction, such as Vegavis and Asteriornis, implies
that the palaeognath-neognath split must have occurred even earlier in the Cretaceous
(though, as described above, molecular divergence dates do not agree on the true antiq-
uity of the basal neornithine phylogenetic divergence).
Longstanding biogeographic hypotheses held that Neornithes originated in Gond-
wana [26,55], partly on the basis that there are far more extant endemic bird clades on the
southern continents of South America, Africa, and Australia than there are on the northern
continents of North America and Eurasia [455]. However, the discovery of Asteriornis in
Europe indicates that deeply diverging crown bird lineages have a long evolutionary his-
tory in the Northern Hemisphere [72]. More broadly, many clades that are currently re-
stricted to tropical latitudes have fossil stem group representatives in the Paleocene and
Eocene of the Northern Hemisphere (e.g., [70,74,120,124,455–457]), implying far more
widespread geographic distributions early in these clades’ evolutionary histories. Given
the generally dispersive capacity of birds, as well as the fact that hothouse climatic condi-
tions predominated throughout the early Paleogene and led to the expansion of paratrop-
ical forests into high latitudes, the present-day geographic distributions of many extant
tropical clades may not reliably indicate their ancestral areas of origin [74]. In light of these
considerations, determining the most likely fossil localities for revealing the first evidence
of a Cretaceous stem palaeognath is challenging, and it would seem equally probable that
an early palaeognath could derive from Late Cretaceous deposits of either the northern or
the southern hemisphere.
4.2. Stem Group Representatives of Extant Palaeognath Subclades
If contemporary hypotheses of ratite paraphyly and dispersal are accurate, small vo-
lant palaeognaths should have been present on landmasses where extant palaeognaths
are found during the Paleocene or Eocene [45]. However, the timing of each independent
palaeognath transition to large body size and flightlessness is uncertain. Transitions to
complete flightlessness among island-dwelling birds typically necessitate few terrestrial
predators and a food source that does not require flight [458,459]. If these conditions are
met, flightlessness may be advantageous because it allows for energy conservation
through reduction in the size of the pectoral musculature [460]. Indeed, the basal meta-
bolic rates of flightless rails are lower than those of closely related flighted rails [460].
Given the right circumstances, transitions to flightlessness and large body size can appar-
ently arise quite rapidly. The extinct giant flightless Hawaiian goose Branta rhuax is nested
within the Canada Goose Branta canadensis species complex, and its presence on the main
Diversity 2022, 14, 105 51 of 70
island of Hawai’i means it must have become large and flightless in less than 500,000 years
Most geologically recent transitions to avian flightlessness occurred on oceanic is-
lands in the absence of predation and competition from terrestrial mammals [458,459].
Were these conditions met on continents in the wake of the K–Pg mass extinction event,
allowing multiple lineages of ratites to evolve flightlessness and large body sizes before
mammalian predators and competitors could evolve? These conditions appear to have
been met on at least some landmasses, as even 10 million years after the extinction event
most mammals remained relatively small and unspecialized [462]. The Corral Bluffs site
in Colorado suggests that the mammalian fauna in the immediate aftermath of the K–Pg
was dominated by small omnivores and insectivores [463], and generally there was a
dearth of specialized mammalian carnivores in the early Paleocene [76,464,465]. The
makeup of terrestrial mammalian faunas at the time could well have favoured the evolu-
tion of flightlessness in birds that could obtain food on the ground, and other large flight-
less Paleogene bird clades such as Gastornithidae, Phorusrhacidae, and Dromornithidae
may have followed a similar pattern along with ratites [76]. In particular, the lack of pla-
cental carnivores in South America through most of the Cenozoic may have contributed
to the diversity of flightless birds on that continent, which also included Phorusrhacoidea
and the giant anseriform Brontornis [76].
If volant stem group representatives of various palaeognath subclades evolved into
large-bodied, flightless forms during a relatively narrow temporal window in the early
Paleogene, the chances of finding direct fossil evidence of these small-bodied ancestral
forms might be relatively low. Indeed, short internodes near the root of Notopalaeog-
nathae indicate a rapid diversification of palaeognath lineages during the Paleogene
[41,56]. However, if some transitions to flightlessness were protracted, the chances of
identifying informative fossils documenting such transitions would be more likely. With
their recent reassignment to total clade Struthionidae, eogruids are a superb example of
previous unrecognised stem group representatives of an extant ratite lineage, though bet-
ter data on their wing apparatus are needed in order to assess whether all known taxa
were flightless. If some taxa were volant, Eogruidae could provide an illuminating win-
dow into the relative timing of transitions to cursoriality, large body size, and loss of flight
in a ratite lineage.
A further challenging aspect of reconstructing the early evolutionary history of the
various ratite lineages is that, if flightlessness and large body size arose numerous inde-
pendent times, confidently assigning a given volant palaeognath fossil from the Paleogene
to the correct palaeognath subclade may prove difficult due to convergence. However,
the ongoing exploration of certain localities may yield further insight into transitions to
flightlessness among certain ratite lineages—for example, additional finds from the St.
Bathans fauna could shed more light on the origins of moa and kiwi, and help elucidate
whether the stem kiwi Proapteryx was indeed small and volant as initially hypothesized
5. Reconstructing the Most Recent Common Ancestor of Palaeognaths
Understanding the nature of the most recent common ancestor (MRCA) of extant
palaeognaths will reveal much about palaeognath macroevolution, and neornithine mac-
roevolution more broadly. For instance, insight into the flight apparatus of the crown pal-
aeognath MRCA will help explain how the geographic distributions of extant palaeog-
naths arose. Moreover, stem palaeognaths (along with stem galloanserans and stem neo-
avians) are inferred to have survived the end-Cretaceous mass extinction event
[41,48,71,72], while all non-neornithine birds appear to have perished [73]. Strong evi-
dence regarding the morphology and ecology of early palaeognaths may also help clarify
ecological factors that may have favoured the survivorship of crown birds with respect to
non-neornithine avialans—one of the more contentious questions in contemporary pal-
aeornithology [71,77]. Inevitably, given that the palaeognath-neognath split is the deepest
Diversity 2022, 14, 105 52 of 70
divergence within crown birds, a better understanding of the nature of the palaeognath
MRCA will in turn shed light on the common ancestral condition of all extant birds. Alt-
hough much remains to be learned, there are several inferences that can be made regard-
ing the nature of the most recent common ancestor (MRCA) of palaeognaths based upon
the information currently available.
5.1. The Flight Apparatus of the Crown Palaeognath MRCA
Due to the relaxation of stabilizing selection, significant polymorphism exists in the
wing musculature of ratites [466], complicating attempts to infer features of the ancestral
crown palaeognath wing. As the only extant flighted palaeognaths, tinamids presumably
provide the best source of data on the muscular anatomy of the wings of early flighted
palaeognaths. Nearly all flight muscles present in neognaths are found in tinamids, with
the exception of the biceps slip [274,467,468]. Extant phylogenetic bracketing [469] there-
fore indicates that the same suite of muscles would be expected to be present in both the
crown palaeognath and crown neornithine MRCAs. Of course, tinamids are specialized
for burst flight over relatively short distances, and as such are probably imperfect ana-
logues of the ancestral crown palaeognaths that must have colonized distant landmasses
in the early Cenozoic [470]. Subsequent losses of dispersal capacity, and the extinction of
dispersive ancestral lineages, can leave the inaccurate impression that poorly dispersive
taxa underwent oceanic dispersal via stochastic events. For example, the phasianid galli-
forms Margaroperdix (Madagascar) and Anurophasis (New Guinea) are poor dispersers, yet
are found on isolated islands [470]. Phylogenomic analyses revealed that these taxa are
nested within Coturnix quails and likely evolved from a dispersive Coturnix-like ancestor.
Both taxa apparently independently evolved towards a non-dispersive partridge-like
morphotype, reminiscent of how the ratite condition appears to have repeatedly evolved
in palaeognaths [470]. As discussed in this review, some lithornithids appear to have been
reasonably capable fliers and could provide more accurate insight into the nature of dis-
persive ancestral crown palaeognaths.
5.2. Inferred Ecology of the Palaeognath MRCA and K–Pg Survivorship
Non-neornithine avialans thrived throughout the Cretaceous and remained diverse
through the Maastrichtian, before suddenly disappearing at the K–Pg boundary [73]. Un-
til this point, Enantiornithes were the dominant Mesozoic avialan clade with more than
60 known species and a worldwide distribution [471–473]. Why did they become extinct,
while neornithines survived? The answer may be associated with their ecology and habi-
tat preferences. The K–Pg impact was devastating to the world’s forests and resulted in
significant species turnover [71,77,474–478]. Palynology of K–Pg boundary sections across
the globe indicates that ground cover following the impact consisted primarily of ferns.
This “fern spike” is interpreted as evidence of a disaster flora following the destruction of
forests worldwide [71,464,474–476] by widespread fires ignited by the impact and subse-
quent cold and darkness [479,480]. This fern spike persisted for approximately 1,000 years,
and closed-canopy forests appear to have remained generally rare during this interval
[481]. Indeed, it may have taken as long as 1.4 Ma for floral diversity hotspots to reappear
[482]. This widespread habitat destruction would have been a powerful agent of selection
against the mostly arboreal Enantiornithes, though this hypothesis does not explain the
extinction of contemporaneous marine avialans such as Ichthyornithes and Hesper-
ornithes. Instead, the demise of these marine piscivorous taxa may have been part of a
broader collapse of marine food chains in the aftermath of the Chicxulub impact
[77,81,483–486]. Importantly, ancestral state reconstructions of crown birds predict that
the MRCAs of crown birds and the deepest crown bird subclades (Neornithes, Palaeog-
nathae, Neognathae, and Neoaves) were all non-arboreal [71]. As such, the ancestors of
palaeognaths may have made it through this mass extinction event partly by virtue of
having exhibited terrestrial non-arboreal lifestyles.
Diversity 2022, 14, 105 53 of 70
As the most stemward palaeognaths known [49,64], lithornithids provide the best
opportunity to draw fossil-informed inferences about the nature of the crown paleognath
MRCA. Vibrotactile bill tips in Lithornis promiscuus and Paracathartes howardae may have
been associated with probe-feeding in the ground, an interpretation congruent with the
hypothesis of predominant K–Pg survivorship among non-arboreal taxa. A vibrotactile
bill tip organ composed of mechanoreceptors known as Herbst corpuscles embedded
within the bone was hypothesized to be a plesiomorphy of Neornithes by du Toit, et al.
[80], which would support the neornithine MRCA and its immediate descendants as hav-
ing been ground-foraging birds. Such organs are found in palaeognathous and neogna-
thous probe-foragers, enabling them to locate prey buried in substrate through vibration
detection [487,488]. In non-probe-foraging palaeognaths, the vibrotactile bill tip organ is
vestigial [80,489]. The hypothesis that lithornithids and the palaeognath MRCA were
probe-feeders agrees with ideas put forth by Houde [62], who suggested that lithornithids
may have preferred to live near water and probed for food using their long beaks, noting
the similarity of their jaw apparatus to those of kiwi. Additionally, the genus Lithornis
appears to have had relatively large olfactory lobes, similar to olfactory foraging taxa in-
cluding Procellariiformes and kiwi [490]. Since ground feeding birds are more likely to
become flightless than arboreal taxa, a volant, non-arboreal, probe-feeding taxon would
seem to be a provide a reasonable expectation for the ecology of the MRCA of crown pal-
6. Conclusions
Our understanding of palaeognath evolution has progressed markedly over the past
two decades thanks to the development and application of sophisticated molecular phy-
logenetic approaches and the continued interrogation of the fossil record; however, many
fundamental questions about the origins of extant palaeognath diversity remain unan-
swered. The present review affirms that the palaeognath crown group has a reasonably
thorough fossil record from the late Oligocene-early Miocene onwards, with the exception
of early elephant birds and early representatives of the New Zealand ratites, whose fossil
record remains sparse until the Pleistocene [392,397,409]. However, the fossil record still
fails to clearly illuminate how and when independent transitions to large body size and
flightlessness arose among the multiple lineages of “ratites”. As yet, volant stem members
of these extant flightless clades remain unknown (besides the possible exception of Pro-
apteryx [387]), leaving the early evolutionary history of crown group palaeognaths
shrouded in mystery. Lithornithids currently provide the best insight into the nature of
the earliest total-clade palaeognaths, and their relatively small size, probable non-arboreal
ecology, and apparent capacity for sustained flight may make them useful models for un-
derstanding the nature of avian survivors of the end-Cretaceous mass extinction event. In
the coming years, we anticipate increased consensus on both the evolutionary relation-
ships and age of Palaeognathae and its major subclades, and hope that such advances are
accompanied by the recognition of new fossil total-group palaeognaths from the Mesozoic
and early Cenozoic. Such advances will be necessary to fill the many gaps in the palaeog-
nath fossil record identified in this review, and to shed light on the repeated independent
origins of “ratites”—one of the most striking examples of convergent evolution in birds,
or indeed any other vertebrate clade.
Author Contributions: Conceptualization, K.W. and D.J.F.; methodology, K.W. and D.J.F. investi-
gation, K.W.; data curation, K.W.; writing—original draft preparation, K.W.; writing—review and
editing, K.W. and D.J.F.; visualization, K.W.; supervision, D.J.F.; funding acquisition, K.W. and
D.J.F. All authors have read and agreed to the published version of the manuscript.
Funding: This research was funded by UKRI Future Leaders Fellowship, grant number
MR/S032177/1 to D.J.F.
Institutional Review Board Statement: Not applicable.
Diversity 2022, 14, 105 54 of 70
Acknowledgments: We thank E. Buffetaut and D. Angst for the opportunity to contribute to this
Special Issue, K. Welch for proofreading, and G. Mayr as well as an anonymous reviewer for con-
structive comments on our manuscript.
Conflicts of Interest: The authors declare no conflict of interest. The funders had no role in the
design of the study; in the collection, analyses, or interpretation of data; in the writing of the manu-
script, or in the decision to publish the results.
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