Augmenting Trait-Dependent Diversification Estimations with Fossil Evidence: A Case Study Using Osmoregulatory Neurovasculature

Abstract

When comparative neuromorphological studies are extended into evolutionary contexts, traits of interest are often linked to diversification patterns. Features demonstrably associated with increases in diversification rates and the infiltration or occupation of novel niche spaces are often termed “key innovations.” Within the past decade, phylogenetically informed methods have been developed to test key innovation hypotheses and evaluate the influence these traits have had in shaping modern faunas. This is primarily accomplished by estimating state-dependent speciation and extinction rates. These methods have important caveats and guidelines related to both calculation and interpretation, which are necessary to understand in cases of discrete (qualitative) character analysis, as can be common when studying the evolution of neuromorphology. In such studies, inclusion of additional characters, acknowledgement of character codistribution, and addition of sister clade comparison should be explored to ensure model accuracy. Even so, phylogenies provide a survivor-only examination of character evolution, and paleontological contexts may be necessary to replicate and confirm results. Here, I review these issues in the context of selective brain cooling – a neurovascular-mediated osmoregulatory physiology that dampens hypothalamic responses to heat stress and reduces evaporative water loss in large-bodied mammals. This binary character provides an example of the interplay between sample size, evenness, and character codistribution. Moreover, it allows for an opportunity to compare phylogenetically constrained results with paleontological data, augmenting survivor-only analyses with observable extinction patterns. This trait- dependent diversification example indicates that selective brain cooling is significantly associated with the generation of modern large-mammal faunas. Importantly, paleontological data validate phylogenetic patterns and demonstrate how suites of characters worked in concert to establish the large-mammal communities of today.

High‐Resolution Computed Tomography Imaging of the Cranial Arterial System and Rete Mirabile of the Cat (Felis catus)

“…A fully developed rete has been described in the cat, as well as in the sheep, goat (Capra hircus), ox (Bos taurus), and pig (Sus scrofa), and other artiodactyls, with a rudimentary one in the dog (Canis familiaris) (Gillilan, 1974;Gillilan, 1976;Strauss et al, 2017;O'Brien, 2018aO'Brien, , 2018b. There is no rete in the rabbit (Oryctolagus cuniculus) and rat (Rattus norvegicus) (Daniel et al, 1953).…”

“…Recent publications have extensively reviewed these topics, focusing on the various physiological roles of the carotid rete, including water conservation through selective brain cooling mechanisms and the history of multiple different evolutionary modifications (O'Brien, 2015;Strauss et al, 2017;O'Brien, 2018aO'Brien, , 2018b. Although these authors focus on even-toed ungulates, they note that the rete mirabile was first studied in the cat.…”

“…There is a very long history of extensive continuing interest in the anatomy and the role of the rete mirabile of the cat and other mammals, going back to Galen in the second century AD (Baker, 1972;de Gutterez-Mahoney and Schechter, 1972;McFarland et al, 1979) and even earlier ascribed to Herophilus in the third century BC (de Gutterez-Mahoney and Schechter, 1972;McFarland et al, 1979). The large past literature dealing with the rete mirabile has been extensively discussed in recent publications that focus on the various physiological roles of the rete mirabile, including water conservation through selective brain cooling mechanisms (O'Brien, 2015;Strauss et al, 2017;O'Brien, 2018aO'Brien, , 2018b. The large number of publications studying the rete mirabile in the cat likely relates to the fact that the cat was one of the common laboratory subjects (Gillilan and Markesbery, 1963).…”

“…Recent publications have extensively reviewed these topics, focusing on the various physiological roles of the retia, including water conservation through selective brain cooling mechanisms (O'Brien, 2015;Strauss et al, 2017;O'Brien, 2018aO'Brien, , 2018b.…”

How does homeostasis happen? Integrative physiological, systems biological, and evolutionary perspectives

“…Heat transfer occurs when relatively cool venous blood from the nasopharyngeal mucosa flows into the pterygoid plexus surrounding the carotid rete mirabile at the base of the brain. Delivery of blood that is cooler than the core temperature could also result in decreased sweating in a hot environment and consequently provide a mechanism for water preservation (124,153). The rete mirabile dampens blood pressure oscillations at the level of the brain, and this could be important in the giraffe when the animal stoops to drink and the brain is below the level of the heart.…”