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Title:The evolutionary transition from reptiles to mammals: analyses of body size reduction and separation of middle ear elements from the jaw
Author(s):Urban, Daniel Joseph
Director of Research:Sears, Karen
Doctoral Committee Chair(s):Sears, Karen
Doctoral Committee Member(s):Marcot, Jonathan; Frazzetta, Thomas; Roseman, Charles; Luo, Zhe-Xi
Department / Program:School of Integrative Biology
Degree Granting Institution:University of Illinois at Urbana-Champaign
Body Size
Middle Ear
Meckel's Cartilage
Abstract:Body size generally decreased during synapsid evolution until the origin of mammals, and this decrease has often been linked to the evolution of mammal-like characteristics. Despite the importance of these patterns to our understanding of mammalian evolution, the particular evolutionary mechanisms that underlie them are less clear. Previous studies have tested models across synapsid phylogeny prior to the origin of mammals and found little evidence for a pervasive direction bias in body size evolution. However, whether the rate or mode of body size evolution changed among particular subclades, or after the origin of mammals, has not been explored quantitatively. In this study we constructed a phylogenetic framework and used two proxies for body size (humerus and femur length) to model the pattern of body size evolution in a diverse suite of non-mammalian synapsids and Mesozoic mammals. Specifically, we statistically tested for shifts in the rates or modes of body size evolution at specific times or nodes of the phylogeny. Results confirm that passive processes are responsible for body size reduction when viewing the phylogeny as a whole. However, there is evidence of multiple rate changes along the way, as well as a significant period of stasis in the small early mammals. Body size also tended to evolve at a slower rate in mammals than in their ancestors. These results suggest that mammals exhibited significantly different evolutionary dynamics than their synapsid ancestors, consistent with a selective advantage for small body size in these groups. The evolutionary transition from reptiles to mammals is characterized by many remarkable changes, perhaps none more dramatic than the conversion of postdentary elements from the reptilian jaw into the middle ear of mammals. Reptiles and early synapsids possess multiple bones in the jaw but only a single bone in the middle ear, the columella (stapes). Additionally, they conduct jaw abduction via a joint between the articular and the quadrate. Conversely, mammals all possess a single bone in the jaw, the dentary, and multiple bones in the middle ear. Mammalian jaw articulation takes place between the dentary and squamosal. Throughout evolutionary history mammals have formed a new jaw joint and extended the middle ear into a three-ossicle chain. The articular and quadrate of the reptilian jaw have become the malleus and incus of the mammalian middle ear, respectively, adding to the pre-existing stapes. Another homologous element in this transition is the ectotympanic ring, which originated from the angular in the mandible. The historical transformation of these bones is documented in the fossil record, though gaps remain. In order to help elucidate some of the existing gaps, we studied the transition of these elements in the development of an extant mammal. Modern marsupials are born in an extremely premature state. In fact, at the time of birth they still exhibit a reptilian-style jaw joint between the articular and quadrate. Not until postnatally does the new jaw joint form and the original elements transition to the typical mammalian positioning within the middle ear. We utilized micro-CT scans of neonatal Monodelphis domestica taken at five-day intervals throughout the first month and a half of postnatal development to use as comparisons with exceptional fossil specimens from the past 250 million years. Three-dimensional reconstructions from these developmental time points line up quite well with the fossil record. Each five-day increment in early development equates with an approximate 40-million year jump in the fossil record. We also find that the Meckel’s cartilage, connecting the dentary to malleus, begins to separate at 20 days postnatal. This marks a significant milestone in development, as it is the point at which the middle ear ossicles gain independence from the jaw and can become specialized for hearing. Derived elements, such as the manubrium of the malleus, develop much later, consistent with their subsequent appearance in the fossil record after the origin of mammals. Overall, marsupial development appears to recapitulate evolutionary transitions within the synapsid lineage leading to mammals. The middle ear ossicles did not separate from the jaw in a single step, but rather underwent a distinct two-step process. Several exceptionally preserved fossils from ~120mya, Yanoconodon and Liaoconodon, show us that the first step consisted of a mediolateral separation of the elements from the dentary while they maintained an anterior connection via an ossified Meckel's cartilage. Only in later organisms did the MC become absorbed, completing the second step of the separation. It was this final degeneration of the Meckel’s cartilage that fully freed the middle ear elements from their association with the jaw and allowed unconstrained evolution for improvement hearing functionality. While the fossil record documents the middle ear transition through time, it only gives us a view of the patterns of change, leaving the underlying processes as a mystery. In order to fully understand the mechanistic drivers of such a dramatic shift, we need to examine the transition in an extant organism. Marsupials offer an opportunity for just such an analysis as their postnatal development essentially recapitulates the entire transition as observed in the fossil record. Thus, using Monodelphis we strove to uncover the underlying cellular and genetic drivers that are responsible for the separation of middle ear elements from the jaw. As we previously noted, the timeframe of Meckel’s disconnection from the malleus at postnatal day 20 served as a starting point for this work. Immunohistochemical staining revealed, that contrary to what is observed in placental mammals, apoptosis places an essential role in degenerating MC at the point of connection with the malleus. Programmed cell death has been ruled out as a factor in Meckel's breakdown for placentals, making it a comparatively novel method for marsupials to complete the same process. Interestingly, RNA-sequencing revealed significant upregulation in a handful of key genes (including Tgfbr2, Wisp1, Mmp9 and Ctsk) responsible for promoting apoptosis, bone breakdown, and cartilage resorption. Through verification with fluorescent in situ hybridization (FISH), all of these factors were shown to increase in expression level as they approached day 20. Inhibiting gene expression through anti-TGFb and alendronate injections, in order to prohibit apoptosis and osteoclast formation, resulted in maintenance of the Meckel's cartilage connection beyond the 20-day mark, and indications of MC ossification as well. An ossified MC was also evident in several ancestral lineages, indicating that changes in expression level of just a few genes may have been all that was required for independence of the middle ear elements.
Issue Date:2016-04-14
Rights Information:Copyright 2016 Daniel Urban
Date Available in IDEALS:2016-07-07
Date Deposited:2016-05

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