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. 2021 Sep 6:9:e12094.
doi: 10.7717/peerj.12094. eCollection 2021.

Phylogenetic analysis of a new morphological dataset elucidates the evolutionary history of Crocodylia and resolves the long-standing gharial problem

Jonathan P Rio  1 , Philip D Mannion  2
Affiliations

Phylogenetic analysis of a new morphological dataset elucidates the evolutionary history of Crocodylia and resolves the long-standing gharial problem

Jonathan P Rio et al. PeerJ. .

Abstract

First appearing in the latest Cretaceous, Crocodylia is a clade of semi-aquatic, predatory reptiles, defined by the last common ancestor of extant alligators, caimans, crocodiles, and gharials. Despite large strides in resolving crocodylian interrelationships over the last three decades, several outstanding problems persist in crocodylian systematics. Most notably, there has been persistent discordance between morphological and molecular datasets surrounding the affinities of the extant gharials, Gavialis gangeticus and Tomistoma schlegelii. Whereas molecular data consistently support a sister taxon relationship, in which they are more closely related to crocodylids than to alligatorids, morphological data indicate that Gavialis is the sister taxon to all other extant crocodylians. Here we present a new morphological dataset for Crocodylia based on a critical reappraisal of published crocodylian character data matrices and extensive firsthand observations of a global sample of crocodylians. This comprises the most taxonomically comprehensive crocodylian dataset to date (144 OTUs scored for 330 characters) and includes a new, illustrated character list with modifications to the construction and scoring of characters, and 46 novel characters. Under a maximum parsimony framework, our analyses robustly recover Gavialis as more closely related to Tomistoma than to other extant crocodylians for the first time based on morphology alone. This result is recovered regardless of the weighting strategy and treatment of quantitative characters. However, analyses using continuous characters and extended implied weighting (with high k-values) produced the most resolved, well-supported, and stratigraphically congruent topologies overall. Resolution of the gharial problem reveals that: (1) several gavialoids lack plesiomorphic features that formerly drew them towards the stem of Crocodylia; and (2) more widespread similarities occur between species traditionally divided into tomistomines and gavialoids, with these interpreted here as homology rather than homoplasy. There remains significant temporal incongruence regarding the inferred divergence timing of the extant gharials, indicating that several putative gavialids ('thoracosaurs') are incorrectly placed and require future re-appraisal. New alligatoroid interrelationships include: (1) support for a North American origin of Caimaninae in the latest Cretaceous; (2) the recovery of the early Paleogene South American taxon Eocaiman as a 'basal' alligatoroid; and (3) the paraphyly of the Cenozoic European taxon Diplocynodon. Among crocodyloids, notable results include modifications to the taxonomic content of Mekosuchinae, including biogeographic affinities of this clade with latest Cretaceous-early Paleogene Asian crocodyloids. In light of our new results, we provide a comprehensive review of the evolutionary and biogeographic history of Crocodylia, which included multiple instances of transoceanic and continental dispersal.

Keywords: Allgatoroidea; Continuous characters; Crocodylia; Crocodyloidea; Extended implied weighting; Gavialoidea; Gharial problem; Phylogeny.

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Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Figure 1
Figure 1. Simplified cladogram of Crocodylomorpha, after Wilberg, Turner & Brochu (2019).
Figure 2
Figure 2. Cladograms outlining the interrelationships of extant crocodylians implied from the taxonomic classification schemes of earlier studies.
(A) After Romer (1956) and Steel (1973); (B) after Kälin (1955) and Sill (1970); (C) after Mook (1934); and (D) after Hay (1930).
Figure 3
Figure 3. Simplified interrelationships of Crocodylia based on the phenogram generated by Densmore (1983).
Figure 4
Figure 4. Simplified cladogram, illustrating the traditional morphological hypothesis of extant crocodylian interrelationships.
Figure 5
Figure 5. Contrasting topologies of molecular (A) and morphological (B) phylogenies illustrating differences in the divergence of principal crocodylian clades.
Molecular divergences based on Oaks (2011) and morphological divergences based on the stratigraphically oldest fossils assigned to each clade prior to the current study.
Figure 6
Figure 6. Time-calibrated phylogenies illustrating the stratigraphic distribution of (A) Gavialoidea after Salas-Gismondi et al. (2019), and (B) Tomistominae after Jouve (2016).
Taxa in grey not included in aforementioned studies.
Figure 7
Figure 7. Simplified morphological phylogeny of Crocodylia based on Brochu et al. (2012), summarising some of the taxonomic problems discussed.
Figure 8
Figure 8. A summary of terms used to categorise synapomorphies.
Red branches highlight the ingroup.
Figure 9
Figure 9. Summary of phylogenetic results from all nine analyses.
Figure 10
Figure 10. The strict consensus of the three most parsimonious trees obtained from Analysis 1.3.
Values adjacent to nodes indicate values of internal consistency (Bootstrap/Jackknife/Bremer) and are shown only for nodes with Bremer support over 1 average step length.
Figure 11
Figure 11. Time-calibrated phylogeny of stem crocodylian taxa from Analysis 1.3.
Ages = Ma. Support values: Bootstrap/Jackknife/Bremer. Abbreviations: As, Asia; Aust, Australasia; Eur, Europe; NA, North America.
Figure 12
Figure 12. Time-calibrated phylogeny of Alligatoroidea from Analysis 1.3.
Ages = Ma. Support values: Bootstrap/Jackknife/Bremer. Abbreviations: As, Asia; Eur, Europe; NA, North America; SA, South America.
Figure 13
Figure 13. Caiman lutescens (MACN PV 13551) skull in (A) dorsal view, and (B) dorsolateral view.
Figure 14
Figure 14. Occipital view of the cranium showing variation in morphology of the posterior cranial table margin.
(A) Caiman yacare (AMNH 97300); (B) Caiman lutescens (MACN PV 13551); (C) Purussaurus neivensis (UCMP 39704); (D) Caiman gasparinae (right hand side mirrored for clarity) (MLP-IV-15-1); (E) Purussaurus neivensis juvenile (IGM DHL-45); (F) Mourasuchus arendsi (UFAC 1431). All scale bars = 20 mm.
Figure 15
Figure 15. Anterolateral view of the rostrum showing morphology of the interorbital bridge (spectacle).
(A) Caiman lutescens (MACN PV 13551); (B) Mourasuchus arendsi (UFAC 5883); (C) Melanosuchus niger (NHMUK 45.8.25.125); (D) Purussaurus neivensis (UCMP 39704). Scale bar in A = 50 mm.
Figure 16
Figure 16. UCMP 39978 (‘Caiman cf. lutescens’) skull in (A) dorsal; (B) ventral; and (C) left lateral views.
Scale bar = 50 mm.
Figure 17
Figure 17. Time-calibrated phylogeny of Gavialoidea.
Ages = Ma. Support values: Bootstrap/Jackknife/Bremer. Abbreviations: Af, Africa; As, Asia; CA, Central America; Eur, Europe; NA, North America.
Figure 18
Figure 18. Simplified cladograms illustrating alternative optimisations of a hypothetical character on a morphological (A) and molecular (B) tree.
Figure 19
Figure 19. Simplified phylogeny illustrating the topology recovered by Narváez et al. (2016).
Stars indicate the nodes for which synapomorphies were optimised.
Figure 20
Figure 20. Simplified cladograms illustrating the principal changes in character optimisation of synapomorphies of Brevirostres and stemwards nodes recovered in Narváez et al. (2016).
For simplicity, ’outgroup’ refers to all taxa stemward of Borealosuchus recovered here. See text for further explanation.
Figure 21
Figure 21. Synapomorphies of Gavialoidea and less inclusive clades that unite morphological (=traditional) tomistomines and gavialoids.
Figure 22
Figure 22. Strict consensus of the three MPTs resulting from Analysis 1.3 with ‘thoracosaurs’ constrained to be excluded from Crocodylia.
Crown gavialids highlighted in red, ‘thoracosaurs’ highlighted in blue.
Figure 23
Figure 23. Strict consensus of the three MPTs resulting from Analysis 1.3 with ‘thoracosaurs’ constrained to be excluded from Gavialidae.
Crown gavialids highlighted in red, ‘thoracosaurs’ highlighted in blue.
Figure 24
Figure 24. Strict consensus of the three MPTs resulting from Analysis 1.3 with ‘thoracosaurs’ constrained to be excluded from Crocodylia, but with Eogavialis and Argochampsa allowed to float.
Crown gavialids highlighted in red, ‘thoracosaurs’ highlighted in blue.
Figure 25
Figure 25. Time-calibrated phylogeny of Crocodyloidea from Analysis 1.3.
Ages = Ma. Support values: Bootstrap/Jackknife/Bremer. Abbreviations: As, Asia; Aust, Australasia; CA, Central America; Eur, Europe; Ind, Indo-Pacific (Malay Archipelago); NA, North America; SA, South America.
Figure 26
Figure 26. The distribution of named species referred to Hylaeochampsidae.
Global palaeogeographical reconstruction at 125 Ma from Fossilworks (http://fossilworks.org/) (Alroy, 2013) based on data in the Paleobiology Database (https://paleobiodb.org/).
Figure 27
Figure 27. The distribution of named species referred to Allodaposuchidae and Borealosuchus.
Global palaeogeographical reconstruction at 66 Ma from Fossilworks (http://fossilworks.org/) (Alroy, 2013) based on data in the Paleobiology Database (https://paleobiodb.org/).
Figure 28
Figure 28. The distribution of named alligatoroids in the Paleocene.
Global palaeogeographical reconstruction at 60 Ma from Fossilworks (http://fossilworks.org/) (Alroy, 2013) based on data in the Paleobiology Database (https://paleobiodb.org/).
Figure 29
Figure 29. The distribution of named and valid alligatoroid species in the Eocene.
Global palaeogeographical reconstruction at 40 Ma from Fossilworks (http://fossilworks.org/) (Alroy, 2013) based on data in the Paleobiology Database (https://paleobiodb.org/).
Figure 30
Figure 30. Summary of possible paleobiogeographic routes available from the latest Cretaceous–early Paleogene, after Brikiatis (2014).
Global palaeogeographical reconstruction centered on the North Pole at 66 Ma from Fossilworks (http://fossilworks.org/) (Alroy, 2013). Star indicates the location of an indeterminate alligatorid from the early Eocene, based on data in the Paleobiology Database (https://paleobiodb.org/).
Figure 31
Figure 31. The distribution of Alligator.
Global palaeogeographical reconstruction at 6 Ma from Fossilworks (http://fossilworks.org/) (Alroy, 2013) based on data in the Paleobiology Database (https://paleobiodb.org/). Note that only the oldest occurrence of A. mississippiensis is shown, because numerous specimens can be assigned to this species from the Quaternary, all of which approximately fall within its present-day range.
Figure 32
Figure 32. Principal South American fossil localities showing caimanine distribution from the Neogene to the Quaternary.
Based on data in the Paleobiology Database (https://paleobiodb.org/). Extant caimanine range taken from https://www.iucnredlist.org/. Modern map from https://en.wikipedia.org/wiki/Wikipedia:Blankmaps.
Figure 33
Figure 33. The distribution of Planocraniidae.
Arrows indicate possible dispersal routes. Global palaeogeographical reconstruction at 50 Ma from Fossilworks (http://fossilworks.org/) (Alroy, 2013) based on data in the Paleobiology Database (https://paleobiodb.org/).
Figure 34
Figure 34. The distribution of named/distinct crocodyloids in the latest Cretaceous and Paleogene.
Indeterminate remains discussed in text. Based on data in the Paleobiology Database (https://paleobiodb.org/). Modern map from https://en.wikipedia.org/wiki/Wikipedia:Blankmaps. Note that Australosuchus and Baru darrowi are known from sites dated to late Oligocene–early Miocene.
Figure 35
Figure 35. The distribution and biogeographic history of Mekosuchinae.
(A) Global palaeogeographical reconstruction at 50 Ma from Fossilworks (http://fossilworks.org/) (Alroy, 2013) with arrows showing alternative dispersal routes for an Asian origin of Mekosuchinae. (B) the distribution of named mekosuchines in eastern Australia and South Pacific islands from the Neogene and Quaternary. Based on data in the Paleobiology Database (https://paleobiodb.org/). Modern map from https://en.wikipedia.org/wiki/Wikipedia:Blankmaps.
Figure 36
Figure 36. The distribution of named osteolaemines.
Fossil occurrences based on data in the Paleobiology Database (https://paleobiodb.org/), present-day range of Osteolaemus based on Shirley et al. (2015). Modern map from https://en.wikipedia.org/wiki/Wikipedia:Blankmaps.
Figure 37
Figure 37. The distribution of Crocodylus, Neogene to Recent.
Fossil occurrences based on data in the Paleobiology Database (https://paleobiodb.org/), modern ranges taken from https://www.iucnredlist.org/. Modern map taken from https://en.wikipedia.org/wiki/Wikipedia:Blankmaps.
Figure 38
Figure 38. The distribution of named gavialoid species from the Cretaceous to Eocene.
Fossil occurrences based on data in the Paleobiology Database (https://paleobiodb.org/). Modern ranges taken from https://www.iucnredlist.org/. Modern map taken from https://en.wikipedia.org/wiki/Wikipedia:Blankmaps.
Figure 39
Figure 39. The distribution of named gavialoid species from the Oligocene to present day.
Fossil occurrences based on data in the Paleobiology Database (https://paleobiodb.org/). Modern ranges taken from https://www.iucnredlist.org/. Modern map taken from https://en.wikipedia.org/wiki/Wikipedia:Blankmaps.
Figure 40
Figure 40. Alternative biogeographic scenarios for the origin of Neotropical gavialoids.
Global palaeogeographical reconstruction at 50 Ma from Fossilworks (http://fossilworks.org/) (Alroy, 2013) based on data in the Paleobiology Database (https://paleobiodb.org/).
Figure 41
Figure 41. The distribution of named Gavialis species, illustrating alternative biogeographic routes suggested from a close relationship between South American and Asian gavialids.
Global palaeogeographical reconstruction at 2 Ma from Fossilworks (http://fossilworks.org/) (Alroy, 2013) based on data in the Paleobiology Database (https://paleobiodb.org/).
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