Figure 1.
Systematic and temporal distribution of homeotic character transitions in Mammalian groups.
Divergence data after Springer et al[58], Flynn et al[90], Kielan-Jaworowska et al[76]. K-T-Cretaceous-Tertiary boundary.
Table 1.
Primary Gradient–Segmental Identity and Boundaries
Figure 2.
Thoracic and lumbar segmental homeotic trait patterns in mammalian species.
Figure 3.
Homeotic shifts in the catarrhines.
The data show the average segmental midpoint of nerve and plexus origins relative to vertebral segment regionalization (after Filler 1993 [38], some data from Keith 1902 [91]).
Figure 4.
Secondary sacral boundary shifts within the hominiform clade.
(A) Humans appear to retain the original hominiform longer flexible lumbar region. (B) Anatomical reconfiguration results in effective elimination of the lumbar region in Gorilla. (C) Despite a modal number of 5 lumbars, humans may have 4 lumbar but maintain a long flexible lumbar region. (D) Molecular phylogeny suggests that lumbar region shortening in Pan occurred independently and convergently (X-ray in D after Filler 1979 [92]).
Figure 5.
Frame shifting between rib and vertebral segments.
Evidence for independent formation of a parallel segmental identity gradient for ribs that may differ from the vertebral gradient is demonstrated by frame shifting. The synapsid (sy) primitive condition has a principal (capitular) rib head articulating on a pararthrum on the intercentrum (ic) which seems to serve as a morphogenetic “target”. In basal therians (th), there is no intercentrum, but the rib head still articulates between the two centra (pleurocentra) as if the lost intercentral morphogenetic target were still present. The articulation is divided into a pre-pararthrum (red) on the anterior end of the following vertebra (iso-segmental) and a post-pararthrum (orange) on the posterior end of leading vertebra. In the posterior thorax of many eutherians (e.g. Euarchontoglires, the Xenarthran Order Pilosa) and some metatherians, the post-pararthral articulation is lost (post1)-“pre-pararthral dominance”-and the diarthral (blue) articulation is also suppressed in many groups (post2). However in metatherians, the Xenarthran Order Cingulata, Hippopotamidae and Cetacea, it is the pre-pararthrum that is lost-“post-pararthral dominance”-in the posterior thorax so that the capitulum articulates only with the post-pararthrum (ant1). The post-pararthrum may move away from the intervertebral space (ant2). In some groups, the diarthrum is also lost so that the rib (e.g. r9) articulates only with the leading vertebra (T8)-this is seen sporadically in the posterior thorax in myomorph, hystricomorph and anomaluromorph rodents and perissodactyls.
Table 2.
Second Gradient–Rib Head Suppression and Frame Shifting
Figure 6.
Antecedents and relations of the neomorphic laminapophysis in mammals.
(A)-Configuration of diarthrum, pararthrum and intercentrum in synapsids (Ophiacodon) with the entire pararthrum (orange+red)) on the intercentrum (after Williston[80]) (A1), and diapsids[82] (Crocodylus) upper (A2) and (Alligator) lower (A3) thoracic. (B)-Muscle attachments of the laminapophysis. (C) New nomenclature of vertebral articular surfaces and processes in mammals. Blue-diarthrum, red-pre-pararthrum, orange-post-pararthrum, green-NLM.
Figure 7.
Diversity of lumbar transverse processes (LTP) serial homology and NLM morphology in therians.
(A)-There is an independent laminapophysis (NLM) in Erinaceus (Eulipotyphla) that does not split at the thoraco-lumbar transition and is unrelated to the LTP. Erinaceomorphs have no pre-pararthrum on the last ribbed vertebra (post-pararthral dominance) and have a diapophysial LTP. (B)-Typical transition from tri-articulate rib to uni-articulate rib to LTP in Superorder Euarchontoglires. Note splitting of laminapophysis (NLM) (green), loss of the diarthrum (blue), and suppression of the post-pararthrum (orange) to yield a pre-pararthral base for parapophysial LTP (red)–drawing of Macaca (Primates). (C)-Post-pararthral dominance with anterior segmental frame shift in metatherians. (C1)-Diapophysial LTP with absence of prepararthrum and no participation of the post-pararthrum (orange). The last rib articulates only on the vertebra of the preceding segment. Note that the diarthrum transposes from dorsal to the neuraxis to ventral (diarthro-neural transposition). Drawing of Thylacinus. (C2)-Thoraco-lumbar transition in Thylacinus cynocephalus (Metatheria) MCZ 36797 (photo of specimen drawn in C1).
Figure 8.
(A)-Anterior shift at thoraco-lumbar transition: pararthrum entirely on preceding segment with diarthrum on iso-segment. First lumbar transverse process (LTP) (on L1) is bi-segmental (T13+L1). Transitional vertebra (T13) has no capitular rib articulation and no LTP. Macropus rufus (Metatheria) MCZ 6930. (B)-Anterior shift at cervico-thoracic transition: pararthrum entirely on preceding segment (C7) in Sotalia fluviatilis (Cetacea) FMNH 99612. (C)-Posterior shift in the thoracic region: pararthrum entirely on iso-segment and migrated dorsal to the border between the neural arch and the centrum (neuro-central suture)-these two features together are analogous to the condition in archosaurian reptiles. Myrmecophaga tridactyla (Pilosa) FMNH 49342. Oc–occipital, C-cervical, T-thoracic, L–lumbar, di–diarthrum, pa–pararthrum, nc–neuro-central suture, LTP–lumbar transverse process.
Figure 9.
Distinction of laminapophysis from diapophysis (A)–Relation of diarthrum to laminapophysis in Zaglossus (Monotremata) and Erinaceus (Eulipotyphla).
(B)–Relation of diapophysis to laminapophysis in Potamogale (Afrosoricida). (C)–Distinct diapophysis and laminapophysis in Rhizomys sumatrensis (FMNH 98534) (Rodentia). T-thoracic, L–lumbar, di–diarthrum, la–laminapophysis. Blue–diarthrum, red–pre-pararthrum, orange–post-pararthrum, green–NLM.
Figure 10.
Body configuration change in mammalian axial anatomy.
(A)-Monotonous laminapophysis in Monotremata (Tachyglossus aculeata) with no lumbar transverse process. (B)-Laminapophysis split into anteriorly directed metapophysis that slowly drifts medially to engage in sagittalization of the L4/S1 facet and posteriorly directed anapophysis. Large orthapophysial lumbar transverse processes from “third tubercle” of laminapophysial condyle on the arch (Tapirus bairdii, Perissodactyla). m–metapophysis, a–anapophysis, s–sagittalization.
Table 3.
Third Gradient–Duplications and Mirroring
Figure 11.
Laminapophysis and lumbar transverse processes emergence in mammals.
(A)-Emergence of laminapophysis at T3 in Monotremata (Tachyglossus aculeatus) with no lumbar transverse processes (MCZ 25438). (B)-Emergence of orthapophysial lumbar transverse process (arrow) on vertebra also bearing a rib in small ferungulate (typical adult weight 1.5 kg) Tragulus javanicus subrufus (Artiodactyla) FMNH 62824. T-thoracic, L-lumbar.
Figure 12.
Laminapophysial splitting sequence in non-hominiform and hominiform catarrhines.
(A & B)-The laminapophysis splits into anterior metapophysis (**) and posterior anapophysis (*). The anapophysis forms a posteriorly directed styloid process on the arch and does not participate in the emergence of the pre-pararthral positioned parapophysial LTP. Typical euarchontogliran style anatomy in Macaca (Primates) Harvard Peabody N/3587. (C)-The anapophysis (*) forms the lumbar transverse process rather than a styloid process in hominiforms (e.g. non-proconsulid apes and humans)-juvenile Pan troglodytes. NLM-neomorphic laminapophysis, LTP-lumbar transverse process.
Figure 13.
Homeotic mirroring of axial character elements.
(A)–Mirrored repetition of splitting of laminapophysis into anterior metapophysis and posterior anapophysis with associated sagittalization of facet in thoraco-cervical direction in addition to the usual eutherian thoraco-lumbar gradient polarity for this sequence-Myrmecophaga tridactyla (Pilosa) FMNH 49338. (B)–Medio-lateral mirroring of recurved lumbar facet joints–Dasypus novemcinctus (Cingulata) FMNH 60493.
Figure 14.
Multiple homologies for the therian lumbar transverse process (LTP).
Diapophysial LTP: In metatherians with loss of the pre-pararthrum (red) and descent of the diarthrum (blue) onto the centrum (Figure 7C, 20), the LTP is often based on the diarthrum, occurs on the centrum, and incorporates a distal costal element as in Figure 8A. Parapophysial LTP: In most Euarchontoglires, the post-pararthrum (orange) and diarthrum (blue) are lost in the posterior thorax so that the LTP seriates with the pre-parapophysis and may incorporate a distal costal element as in Figure 7B. Orthapophysial LTP: In most ferungulates, the final rib has both a pre-pararthrum (red) and a post-pararthrum (orange) but no diarthrum (blue) as in Figure 11B. However the horizontal septum–which appears to be involved in inducing LTP formation–is dorsal to the neuraxis (see Figure 20) and the LTP is based on the middle portion of the condyle of the laminapophysis (green) (see Figure 6B). Note that the mamillary (metapophysis) and styloid (anapophysis) are still seen as in Figure 10B. The “third tubercle” of the condyle of the laminapophysis is the orthapophysis. Anapophysial LTP: In hominiforms, the LTP derives from the styloid portion of the laminapophysis (green) (see Figures 12C, 18B, 27A) and so carries the insertion of the longissimus muscle that occurs on the styloid on other euarchontoglirans. A similar LTP occurs in the Pholidota as in Figure 17A. Other versions of therian LTPs may involve various components from this basic set.
Table 4.
Fourth Gradient–Lumbar Transverse Process (LTP) Serial Homology
Figure 15.
Impact of septo-neural transposition on euarchontogliran LTP suspension system in hominiforms.
(A)-A convergent architecture in which LTP tips projecting ventral to the intervertebral center of rotation in most Euarchontoglirans, Carnivora, and Metatherians act to resist lumbar hyperextension by engaging and stretching elastic intertransverse ligaments. Stylo-zygoid contacts in many species further limits hyperextension. (B)-The basal hominiform architecture has LTP tips dorsal to the center of rotation and no styloids so both osseo-ligamentous mechanisms to resist gravitational hyperextension in pronograde posture are absent (after Owen 1857[93]).
Figure 16.
Convergent carnivoran version of LTP suspension system.
(A) The LTP tips are ventral to the vertebral bodies, but they originate on the lamina as orthapophyses dorsal to the neuraxis. (B) Heavily built stylo-zygoid contacts are indicated by the arrow (Panthera tigris MCZ 36675). m-mamillary, s-styloid.
Figure 17.
Morphological and homological lumbar transverse process (LTP) classes.
(A)-The pholidotan Manis temminckii (FMNH 35682) has a full septo-neural transposition as in other ferungulates, but differs from the Carnivora in having purely anapophysial LTPs in place of styloid processes and maintaining the LTP tips well dorsal to the neuraxis-a set of features similar to what is seen in hominiforms. Hyperextension is limited by singly or doubly recurved cylindrical zygapophysial joints as in artiodactyls. B-The rodent Lagostomus trichodactylus (FMNH 53704) has the type of ventrally directed slanted LTPs seen in various ferungulate and metatherian groups-the morphology is part of the convergent LTP suspension system class, but the homology is parapophysial.
Figure 18.
Full septo-neural transposition and styloid entrainment as anapophysial LTPs in hominiforms.
(A)-The LTP (lumbar transverse process) in humans differs markedly from related primates. It is dorsal to the position of the spinal canal. It is thick and strong (triangular or box-like cross-section) instead of flat and thin. (B,C)-Styloid comparison. Lateral view of lumbar vertebrae of human, macaque monkey and Proconsul africanus. The human vertebra, like Morotopithecus, appears to demonstrate absence of the styloid process and relocation of the LTP onto the arch of the vertebra at the base of the structure that carries the facet joint. (D) The Middle Miocene proconsulid hominoid Proconsul africanus appears to have the more primitive LTP and styloid as seen in most euarchontoglirans.
Figure 19.
Abrupt homeotic transformation of the stem hominiform species.
(A)-The lumbar vertebra of Morotopithecus bishopi (Early Miocene hominiform hominoid) has a shape and location of the LTP (lumbar transverse process) near the facet joint on the arch of the vertebra. (B)-The absence of a styloid process and the LTP attachment reaches above the pedicle and has the typical hominiform pattern retained in primitive form in modern humans. The pedicle is enlarged-as in humans. (C)-CT scan of modern human lumbar vertebra showing that the Morotopithecus LTP, pedicle, proportions and facet orientation are within the range of modern human architecture. These features suggest that Morotopithecus may have been the original hominiform upright biped as a consequence of a cluster of homeotic mutational events.
Table 5.
Fifth Gradient–Dorso-Ventral Inflexions and Transpositions
Figure 20.
Approximation, inflexion, and transposition of horizontal body planes.
Early synapsid: The horizontal septum (hs) incorporates the ribs and the principal rib head which articulates on the intercentrum (ic) that is in a ventral location between pleurocentra (pc). This places the septum ventral to the neuraxis (nx) and the pleurocentra (Figure 6A1). Therian Septo-Neural Approximation: In therian mammals, the intercentra are lost and the horizontal septum is repositioned to be just ventral to the neuraxis (Figure 7A). Septo-Neural Inflexion Ventrad: In most groups in the Euarchontoglires, the horizontal septum shifts ventrad away from the neuraxis in the lumbar region (Figure 12B). Dorsad inflexions occur sporadically throughout the Theria. Septo-Neural Transposition Dorsad: The horizontal septum is actually transposed to be dorsal to the neuraxis in hominiform hominoids (Figure 18A), the Ferungulata, many groups in the Afrotheria and Xenartha and sporadically in other groups including some rodents (Figure 25B). Diarthro-Neural Transposition: The diarthral plane of tubercular rib heads transposes to be ventral to the neuraxis in many australodelphian metatherians (Figure 7C).
Figure 21.
Laminar articular engagement in the setting of septo-neural transposition.
(A)-Multiplication of facet surfaces for bony contact of laminar structures to resist hyperextension in the small ameridelphian marsupial Didelphis virginianus (MCZ 1069). (B)-Multiplication of facet surfaces with similar effect in Elephas maximus (MCZ 19157) (Proboscidea).
Figure 22.
Laminar articular engagement with opisthocoely in the Perissodactyla.
(A)-opisthocoelous vertebral centra-anteriorly directed ball shaped surface constrains motion so facets lock to prevent hyperextension. Supplementary facets may occur between spinous processes (Equus caballus). (B)-The partial ventral shift modifying an ancestral septo-neural transposition places the horizontal septum co-planar with the neuraxis so the intervertebral foramina are obliterated. The nerves exit through perforations in the pedicle. There are supplementary articulations between the successive expanded pedicles in Equus burchelli (FMNH 101855) and Tapirus bairdii (FMNH 34666). Note fusion of the pararthrum and diarthrum to form a synarthrum in Equus. p-pararthrum, d-diarthrum, i-intrapedicular foramen, a-anapophysis, syn-synarthrum. (C)-Opisthocoely and supplementary articulations at the base of the LTP and at the ventral margin of the vertebral body in Equus burchelli (FMNH 101855). (D)-Opisthocoely and biplanar pitching of the receiving facets in the rhinoceros Ceratotherium simum (FMNH 29174) as in other perissodactyls.
Figure 23.
Laminar articular engagement in the Artiodactyla.
(A, B)-Hippopotamus amphibius (FMNH 22367) demonstrating full septo-neural transposition (septum dorsal to neuraxis) and the double fluted articular system seen in many artiodactyls to block lumbar hyperextension. (C)-Single fluted locking cylinder articulation (as in pholidotans) and orthapophysial LTP [o] in Boocercus eurycerus (MCZ 27850) with preparthrum [p] (rib-bearing) on the same vertebra as is typical in the Artiodactyla. (D)-Double fluted articulation and separate pedicular perforations for the dorsal and ventral ramus of the exiting segmental spinal nerve in Sus scrofa (FMNH 92908).
Figure 24.
Thoracic rigidification for ventilation during flight.
(A)-Arcade of interdigitating linearly extended capitular rib heads articulating with pedicles in Rhinolophus affinis (MCZ 56962). (B)-Costo-diapophysial fusions in Rhinolophus ferrum (FMNH 84499).
Figure 25.
(A)-Myrmecophaga tridactyla (FMNH 49338) (Pilosa, Xenarthra) demonstrating extra lumbar articulations that seem to appear as a consequence of a morphogenetic replication. (B)-Supplementary facets forming at contact points between the medial styloid and the lateral mamillary processes in Hystrix cristata (FMNH 57170) one of the few rodent groups to demonstrate septo-neural transposition.
Table 6.
Functional Pattern 1–Dorsal Compressive
Table 7.
Functional Pattern 2–Ventral Tensioning
Figure 26.
Laminar articular engagement in great apes-Pongo facet locks and Gorilla laminar blocks.
(A)-Lateral view of orangutan lumbar vertebra: the inferior facet is close to the pedicle (compare with human configuration in Figure 18) and a locking extension assures hard bone to bone contact with the superior facet of the next lower vertebra Pongo pygmaeus Harvard Peabody N/1482. (B)-Dorsal view of gorilla vertebra showing the groove on the superior facet and notch in the lamina that that limit extension (Gorilla gorilla Harvard Peabody 9937). (C)-Developing facet lock in juvenile orangutan (Pongo pygmaeus, juvenile, FMNH 53203). (D)-Developing facet block in juvenile gorilla (Gorilla gorilla, juvenile FMNH 18398).
Table 8.
Functional Pattern 3–Dorsal Tensioning
Figure 27.
Anapophysial serial homology of the LTP in hylobatids.
(A)-L1 showing seriation of styloid portion of split laminapophysis to the LTP in juvenile Hylobates cinereus (FMNH 33543). (B)-Transition of split LTP with styloid seriating into the LTP in juvenile Symphalangus syndactylus (FMNH 122725).
Figure 28.
Lumbar extension in Homo and Pan.
(A)-Lumbar extension in human with six lumbar vertebrae. (B)-lumbar flexion in same individual. (C)-Superimposed images in flexion and extension showing that even with six lumbars, most extension takes place between L4 and the sacrum in humans. (D)-Short lumbar spine with heavy iliolumbar ligaments in Pan obliterating lumbar extension thereby accomplishing support for diagonograde postures. (E)-Comparison of lumbar vertebrae in Gorilla, Pan, and Homo (Owen 1857 [93]) showing the thin flat LTP's typical in Pan because of the primacy of ligament suspension under tension for LTP function rather than muscular force transmission as in other hominoids.