Analysis Of Regionalization And Heterogeneity Throughout The Amniote Lineage

The development of the presacral column was a key step in mammalian evolution, often linked to later specializations in behavior and gait that allowed mammals to thrive in a diverse array of ecosystems. Recent research identified previously unrecognized spinal regionalization in extant sauropsids and, associating this trait with the pervasive Homeobox genes, hypothesized that the degree of vertebral regionalization has been constant throughout amniote evolution while only morphological heterogeneity has increased. Jones et al. argue that this hypothesis is short-sighted, as it fails to factor in the morphologies of non-extant mammalian ancestors. To address this disparity Jones et al. analyzed a set of extinct and extant amniotes to quantify spinal regionalization and disparity throughout mammalian evolution. The results of these analyses were then used to determine the relationship between regionalization, heterogeneity, and evolution.

This data was then used to map regionalization throughout the phylogenic tree. Morphological data were collected from sixty-two skeletal specimens of extant amniotes, fossil specimens of fifteen extinct synapsids, and one fossil specimen of an extinct amniote outgroup. The presacral column of each specimen was measured; measurements were primarily taken from scans with few direct measurements taken from large specimens of the extant sample group. A traditional morphometric measuring approach was followed: both linear and angular measurements were collected. Data ordination was used to determine variance within the column, and spinal regionalization was determined based on a “piecewise regression with an Akaike information criterion (AIC)-weighted average of the relative fit of one- to six-region models”. The resulting numerical regionalization scores reflect the number of regions for the taxon. Heterogeneity was quantified as the “logarithm of the mean variance of the morphological measures of each column”.

The relationship between regionalization and heterogeneity was determined based on a PGLS (phylogenic least-squares) regression. OU (Ornstein-Uhlenbeck) modeling and AIC fitting, paired with the Monte Carlo best-fit approximation, were used to track progressive evolutionary changes in heterogeneity, regionalization, and to define region boundaries. The boundaries were then associated with variations in extant taxon to establish homologies. Alone, the regionalization scores from extant amniote specimens appear to support the hypothesis of conserved regionalization, however, basal synapsids and salamanders have low regionalization scores, effectively supporting a hypothesis of progressive regionalization throughout evolution. Heterogeneity also increased throughout synapsid evolution, although the PGLS regression did not indicate a correlation between heterogeneity and regionalization. OU modeling and AIC fitting indicate that regionalization first increased at the base of Therapsida, while the heterogeneity showed no remarkable increase until the Cynodontia. Subsequent increases in regionalization and heterogeneity are also staggered. It is therefore hypothesized that these evolutionary measures evolved independently.

Region boundaries indicate that the ancestral amniote condition is characterized by three regions: this regionalization is retained in salamanders and basal synapsids. Pelycosaurs also possess three distinct regions, however, the positioning of the regional breaks differ from the ancestral condition. Both synapsids and sauropsids developed the fourth region independently, tied to an increase in shoulder mobility due to a reduction of the pectoral, which lead to specialized gaits. Therian mammals evolved to have a fifth region, the rib-less lumbar region, which is widely heterogeneous across specimens and thus likely related to ecological adaptation. This study is the first to quantify regionalization and heterogeneity throughout the amniote lineage. Since regionalization is a distinguishing feature of mammalian taxa, it is important to understand its evolutionary history so that ecological specialization may be tracked throughout the phylogenic tree. This study finds that heterogeneity and regionalization developed independently throughout mammalian evolution, and widely due to changes in the pectoral in response to ecological specialization.