Detecting Mismatch in Functional Narratives of Animal Morphology: A Test Case with Fossils

Abstract

A boom in technological advancements over the last two decades has driven a surge in both the diversity and power of analytical tools available to biomechanical and functional morphology research. However, in order to adequately investigate each of these dense datasets, one must often consider only one functional narrative at a time. There is more to each organism than any one of these form-function relationships. Joint performance landscapes determined by maximum likelihood are a valuable tool that can be used to synthesize our understanding of these multiple functional hypotheses to further explore an organism's ecology. We present an example framework for applying these tools to such a problem using the morphological transition of ammonoids from the Middle Triassic to the Early Jurassic. Across this time interval, morphospace occupation shifts from a broad occupation across Westermann Morphospace to a dense occupation of a region emphasizing an exposed umbilicus and modest frontal profile. The hydrodynamic capacities and limitations of the shell have seen intense scrutiny as a likely explanation of this transition. However, conflicting interpretations of hydrodynamic performance remain despite this scrutiny, with scant offerings of alternative explanations. Our analysis finds that hydrodynamic measures of performance do little to explain the shift in morphological occupation, highlighting a need for a more robust investigation of alternative functional hypotheses that are often intellectually set aside. With this we show a framework for consolidating the current understanding of the form-function relationships in an organism, and assess when they are insufficiently characterizing the dynamics those data are being used to explain. We aim to encourage the broader adoption of this framework and these ideas as a foundation to bring the field close to comprehensive synthesis and reconstruction of organisms.

Stability–Maneuverability Tradeoffs Provided Diverse Functional Opportunities to Shelled Cephalopods

“…However, strictly planktic interpretations for these entire morphogroups are unlikely. While no ectocochleate was likely to be as athletic or maneuverable as most fish or decabrachian cephalopods ( Jacobs and Chamberlain 1996 ; Neil and Askew 2018 ), they would have been able to swim at comparable speeds (within an order of magnitude) compared to extant Nautilus , provided that they could produce rather conservative jet thrust ( Hebdon et al 2021 ; Hebdon, Ritterbush et al 2022 ; Peterman and Ritterbush 2022 ; Ritterbush and Hebdon 2022 ). Swimming speed is probably not the best metric of performance for ectocochleates.…”

“…However, a growing body of work is demonstrating that serpenticones and sphaerocones did not necessarily experience physical constraints that would have confined them to planktic life habits. Serpenticone conchs do not incur much more drag than oxycones of similar size ( Hebdon, Ritterbush et al 2022 ; Peterman and Ritterbush 2022 ). Sphaerocones have been determined to be more efficient moving at lower Reynolds numbers ( Jacobs 1992 ; Jacobs et al 1994 ; Hebdon et al 2021 ; Hebdon, Ritterbush et al 2022 ) and had superior mobility about the vertical axis ( Peterman and Ritterbush 2022 ).…”

“…Serpenticone conchs do not incur much more drag than oxycones of similar size ( Hebdon, Ritterbush et al 2022 ; Peterman and Ritterbush 2022 ). Sphaerocones have been determined to be more efficient moving at lower Reynolds numbers ( Jacobs 1992 ; Jacobs et al 1994 ; Hebdon et al 2021 ; Hebdon, Ritterbush et al 2022 ) and had superior mobility about the vertical axis ( Peterman and Ritterbush 2022 ). Many shapes across the morphospace iteratively reappear ( Bayer and McGhee 1984 ; Monnet et al 2011 ; Monnet, Klug et al 2015 ), suggesting positive adaptive value, even for morphotypes less hydrodynamically favorable than streamlined oxycones.…”

“…A conch's external shape constrains how the living animal interacts with surrounding water during locomotion (i.e., drag, lift, etc. ; Trueman 1940 ; Denton 1974 ; Chamberlain 1976 , 1981 , 1993 ; Jacobs 1992 ; Jacobs et al 1994 ; Jacobs and Chamberlain 1996 ; Naglik, Tajika, et al 2015 ; Hebdon et al 2020 , 2021 ; Peterman, Hebdon et al 2020 ; Peterman, Shell et al 2020 ; Hebdon, Ritterbush et al 2022 ), while internal morphology and coiling parameters influence hydrostatics (i.e., buoyancy, stability, directional efficiency of movement; Fig. 1C ; Saunders and Shapiro 1986 ; Hoffmann et al 2015 ; Peterman, Barton et al 2019 ; Peterman, Mikami et al 2020 ; Peterman, Yacobucci et al 2020 ; Morón-Alfonso et al 2021 ; Peterman et al 2021 ; Peterman and Ritterbush 2022 ).…”

“…3D ) were termed planktic drifters and vertical migrants, respectively. Nektic life habits are supported for oxycones because they generally experience lower hydrodynamic drag (at higher Reynolds numbers) and have superior coasting efficiency ( Jacobs 1992 ; Hebdon et al 2021 ; Hebdon, Ritterbush et al 2022 ; Peterman and Ritterbush 2022 ; Ritterbush and Hebdon 2022 ). However, a growing body of work is demonstrating that serpenticones and sphaerocones did not necessarily experience physical constraints that would have confined them to planktic life habits.…”