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. 2024 Feb 17;7(1):201.
doi: 10.1038/s42003-024-05879-2.

Predatory synapsid ecomorphology signals growing dynamism of late Palaeozoic terrestrial ecosystems

Suresh A Singh  1 , Armin Elsler  2 , Thomas L Stubbs  3 , Emily J Rayfield  2 , Michael J Benton  2
Affiliations

Predatory synapsid ecomorphology signals growing dynamism of late Palaeozoic terrestrial ecosystems

Suresh A Singh et al. Commun Biol. .

Abstract

Terrestrial ecosystems evolved substantially through the Palaeozoic, especially the Permian, gaining much new complexity, especially among predators. Key among these predators were non-mammalian synapsids. Predator ecomorphology reflect interactions with prey and competitors, which are key controls on carnivore diversity and ecology. Therefore, carnivorous synapsids may offer insight on wider ecological evolution as the first complex, tetrapod-dominated, terrestrial ecosystems formed through the late Palaeozoic. Using morphometric and phylogenetic comparative methods, we chart carnivorous synapsid trophic morphology from the latest Carboniferous to the earliest Triassic (307-251.2 Ma). We find a major morphofunctional shift in synapsid carnivory between the early and middle Permian, via the addition of new feeding modes increasingly specialised for greater biting power or speed that captures the growing antagonism and dynamism of terrestrial tetrapod predator-prey interactions. The further evolution of new hypo- and hypercarnivorous synapsids highlight the nascent intrinsic pressures and complexification of terrestrial ecosystems across the mid-late Permian.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1. Synapsid carnivore jaw morpho-functional diversity.
a Jaw shape morphospace. b Jaw functional characters mapped across shape morphospace. (Colour gradient reflects functional character values—see scale.) c Jaw functional morphospace, with arrows showing general functional trends. Point size represents Log10(mm) femur length. N = 122. Jaw silhouettes: 1. Smilesaurus ferox, 2. Sphenacodon ferox, 3. Secodontosaurus obtusidens, 4. Microvaranops parentis, 5. Varanodon agilis, 6. Lycideops longiceps, 7. Lobalopex mordax, 8. Ictidosaurus angusticeps, 9. Procynosuchus delaharpeae, 10. Dimetrodon milleri, 11. Vetusodon elikhulu, 12. Dinogorgon rubidgei, 13. Deuterosaurus biarmicus. 14. Mycterosaurus longiceps. BF biting force, BIA Biarmosuchia, CYN Cynodontia, DIN Dinocephalia, EOT Eothyrididae, GRG Gorgonopsia, MAMA mean anterior mechanical advantage, MAR maximum aspect ratio, MPMA mean posterior mechanical advantage, OMA opening mechanical advantage, OPH Ophiacodontidae, RAO relative articulation offset, RSL relative symphyseal length, RTL relative toothrow length, SA Symphyseal angle, SPH Sphenacodontia (non-therapsid), SR Symphyseal robusticity, THR Therocephalia, VAR Varanopidae. N = 122 taxa. Biarmosuchia, Dinocephalia and Therocephalia silhouettes by Dmitry Bogdanov (vectorized by T. Michael Keesey); all other silhouettes created by S.A.S., but some are vectorised from artwork by Felipe Alves Elias (https://www.paleozoobr.com/), available for academic use with attribution.
Fig. 2
Fig. 2. Synapsid carnivore feeding functional subgroup jaw characteristics.
The feeding functional subgroup jaw functional character (Supplementary Methods) distributions illustrated using violin and box plots. Functional feeding group compositions illustrated using ring plots detailing relative proportions of different taxonomic groups. Violin plots show taxon density. Box plots showing median value and upper and lower quartiles, with whisker illustrating standard deviation. Mean values indicate by black dots. Coloured arrows indicate whether values increase (red) or decrease (blue) relevant jaw functionality. N = 122. Jaw silhouettes (left to right): Varanodon agilis, Tetraceratops insignis, Dimetrodon grandis, Sauroctonus parringtoni, Smilesaurus ferox, Annatherapsidus petri, Tetracynodon darti. BIA Biarmosuchia, CYN Cynodontia, DIN Dinocephalia, EOT Eothyrididae, GRG Gorgonopsia, MAMA mean anterior mechanical advantage, MAR maximum aspect ratio, MPMA mean posterior mechanical advantage, OMA opening mechanical advantage, OPH Ophiacodontidae, RAO relative articulation offset, RSL relative symphyseal length, RTL relative toothrow length, SA Symphyseal angle, SPH Sphenacodontia (non-therapsid), THR Therocephalia, VAR Varanopidae. N = 122 taxa. Biarmosuchia, Dinocephalia and Therocephalia silhouettes by Dmitry Bogdanov (vectorized by T. Michael Keesey); all other silhouettes created by S.A.S., but some are vectorised from artwork by Felipe Alves Elias (https://www.paleozoobr.com/), available for academic use with attribution.
Fig. 3
Fig. 3. The ecofunctional focus of synapsid carnivore functional feeding groups.
Likely prey preferences and capture methods of the raptorial specialist, speed specialist, power shearer functional feeding groups, as suggested by overall interpretation of jaw functional traits. Jaw silhouettes (left to right): Mesenosaurus romeri, Annatherapsidus petri, Aelurognathus tigriceps. DSS deep shearing specialist, FG forceful gripper, GG gracile gripper, GRA grip and rip attacker, PBS power bite specialist, RLA rapid light attacker, SBS shearing bite specialist, SS speed specialist. All silhouettes created by S.A.S.
Fig. 4
Fig. 4. Synapsid carnivore jaw morpho-functional evolution and relative abundance through time.
a Jaw shape and functional morphospace changes through the late Palaeozoic. Morphospace margin colours correspond to colours of the relevant time bin on the stratigraphic chart. b Relative proportions of different taxonomic groups per time bin through the late Palaeozoic. ART Artinskian, ASL Asselian, BIA Biarmosuchia, CAP Capitanian, CHX Changhsingian, CRC Carboniferous rainforest collapse, CYN Cynodontia, DIN Dinocephalia, ECE End-Capitanian extinction, EOT Eothyrididae, GRG Gorgonopsia, GZH Gzhelian, IND Induan, KAS Kasimovian, KUN Kungurian, OE Olson’s extinction, OPH Ophiacodontidae, PENN Pennsylvanian, PTME Permo-Triassic mass extinction, SAK Sakmarian, SPH Sphenacodontia (non-therapsid), ROA Roadian, THR Therocephalia, VAR Varanopidae, WOR Wordian, WUC Wuchiapingian. Biarmosuchia, Dinocephalia and Therocephalia silhouettes by Dmitry Bogdanov (vectorized by T. Michael Keesey); all other silhouettes created by S.A.S., but some are vectorised from artwork by Felipe Alves Elias (https://www.paleozoobr.com/), available for academic use with attribution.
Fig. 5
Fig. 5. Synapsid carnivore jaw shape and functional phylogenetic disparity through the late Palaeozoic.
a Shape and (b) functional sum of variance calculated for each time bin for carnivorous synapsid groups using phylogenetic time-slicing, divided into: (i) Basal synapsids, (ii) Basal therapsids, and (iii) Eutheriodonts. Significant geological events also highlighted. ‘Overall’ represents all carnivorous synapsids. Shaded 95% confidence intervals shown for each curve. N = 122. ART Artinskian, ASL Asselian, BIA Biarmosuchia, BSL Basal-most synapsids (eothyridids, varanopids, and ophiacodonts), CAP Capitanian, CHX Changhsingian, CRC Carboniferous rainforest collapse, CYN Cynodontia, DIN Dinocephalia, ECE End-Capitanian extinction, GRG Gorgonopsia, GZH Gzhelian, IND Induan, KAS Kasimovian, KUN Kungurian, OE Olson’s extinction, PENN Pennsylvanian, PTME Permo-Triassic mass extinction, SAK Sakmarian, SPH Sphenacodontia (non-therapsid), ROA Roadian, THR Therocephalia, WOR Wordian, WUC Wuchiapingian. Biarmosuchia, Dinocephalia and Therocephalia silhouettes by Dmitry Bogdanov (vectorized by T. Michael Keesey); all other silhouettes created by S.A.S., but some are vectorised from artwork by Felipe Alves Elias (https://www.paleozoobr.com/), available for academic use with attribution.
Fig. 6
Fig. 6. Synapsid carnivore feeding functional subgroups through the late Palaeozoic.
a Relative abundance through time of different feeding functional (sub)groups. b Mean body sizes for each feeding functional subgroup through time. c Composition of each functional feeding group by functional subgroup and clade per time bin. Incorporates unsampled lineages using ancestral trait estimation of overall jaw shape and linear discriminant analysis for FFsG classification. Key geological events shown. Epochs are colour coded by period: Carboniferous (green), Permian (orange), and Triassic (purple). N = 122. ART Artinskian, ASL Asselian, BIA Biarmosuchia, CAP Capitanian, CHX Changhsingian, CYN Cynodontia, DIN Dinocephalia, DSS Deep shearing specialist, ECE End-Capitanian extinction, EOT Eothyrididae and assorted Casesauria, ET Early Triassic, FFsG feeding functional subgroup, FG forceful gripper, GG gracile gripper, GRA grip and rip attacker, GRG Gorgonopsia, GZH Gzhelian, IND Induan, KAS Kasimovian, KUN Kungurian, OE Olson’s extinction, OPH Ophiacodontidae, PBS Power bite specialist, Penn Pennsylvanian, PTME Permo-Triassic mass extinction, RLA Rapid light attacker, ROA Roadian, SAK Sakmarian, SBS Shearing bite specialist, SPH Sphenacodontia (non-therapsid), THR Therocephalia, VAR Varanopidae, WOR Wordian, WUC Wuchiapingian. Biarmosuchia, Dinocephalia and Therocephalia silhouettes by Dmitry Bogdanov (vectorized by T. Michael Keesey); all other silhouettes created by S.A.S., but some are vectorised from artwork by Felipe Alves Elias (https://www.paleozoobr.com/), available for academic use with attribution.
Fig. 7
Fig. 7. Synapsid carnivore ecomorphological evolution through the late Palaeozoic.
Feeding functional subgroup states cross the carnivorous synapsid phylogeny with reconstructed ancestral character state likelihoods based on mean recovered states under equal, symmetrical, asymmetrical, and all rates different models of character transition denoted by pie charts at node positions. Positions of key clades indicated by numbers in bold across the phylogeny. Pulses of diversification highlighted with shaded boxes (grey for carnivorous synapsids and pale green for tetrapod herbivores). Body size represented by Log10(mm) femur length, with branch colour denoting low or high values (see scale). Key geological events shown. N = 122. ART Artinskian, ASL Asselian, BIA Biarmosuchia, CAP Capitanian, CHX Changhsingian, CYN Cynodontia, DIN Dinocephalia, DSS Deep shearing specialist, ECE End-Capitanian extinction, EOT Eothyrididae, ET Early Triassic, FFsG feeding functional subgroup, FG forceful gripper, GG gracile gripper, GRA grip and rip attacker, GRG Gorgonopsia, GZH Gzhelian, I Induan, KAS Kasimovian, KUN Kungurian, MOS Moscovian, OE Olson’s extinction, OPH Ophiacodontidae, PBS Power bite specialist, PTME Permo-Triassic mass extinction, RLA Rapid light attacker, ROA Roadian, SAK Sakmarian, SBS Shearing bite specialist, SPH Sphenacodontia (non-therapsid), THR Therocephalia, VAR Varanopidae, WO Wordian, WUC Wuchiapingian. Biarmosuchia, Dinocephalia and Therocephalia silhouettes by Dmitry Bogdanov (vectorized by T. Michael Keesey); all other silhouettes created by S.A.S., but some are vectorised from artwork by Felipe Alves Elias (https://www.paleozoobr.com/), available for academic use with attribution.
Fig. 8
Fig. 8. Feeding functional subgroup and size differentiation within carnivorous synapsid assemblages through the late Palaeozoic.
The feeding functional subgroup classifications and size of carnivorous synapsids within late Palaeozoic fossil assemblages, illustrating potential ecological similarity and changes in niche differentiation. Body size represented by Log10(mm) femur length. *Size based on Permian specimen as Early Triassic specimen with complete femur length measurement could not be sourced—Early Triassic specimens are typically smaller owing to Lilliput effect across the PTME. Key geological events shown. Epochs are colour coded by period: Carboniferous (green), Permian (orange), and Triassic (purple). N = 81. BIA Biarmosuchia, CIST. AZ Cistecephalus Assemblage Zone, CYN Cynodontia, DIN Dinocephalia, DSS Deep shearing specialist, ECE End-Capitanian extinction, END. AZ Endothiodon Assemblage Zone (Lycosuchus—Eunotosaurus subzone), EOT Eothyrididae, E. Tri Early Triassic, FFsG Feeding functional subgroup, FG Forceful gripper, FL Femur length, GG Gracile gripper, GRA Grip and rip attacker, GRG Gorgonopsia, Lcm Locomotion, LYST. AZ Lystrosaurus declivis Assemblage Zone, OE Olson’s extinction, OPH Ophiacodontidae, PBS Power bite specialist, Penn Pennsylvanian, PTME Permo-Triassic mass extinction, RLA Rapid light attacker, SBS Shearing bite specialist, SPH Sphenacodontia (non-therapsid), TAP. AZ Tapinocephalus Assemblage Zone (Diictodon—Styracocephalus subzone), THR Therocephalia, VAR Varanopidae. Biarmosuchia, Dinocephalia and Therocephalia silhouettes by Dmitry Bogdanov (vectorized by T. Michael Keesey); all other silhouettes created by S.A.S., but some are vectorised from artwork by Felipe Alves Elias (https://www.paleozoobr.com/), available for academic use with attribution.
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