Wing musculature reconstruction in extinct flightless auks (PinguinusandMancalla) reveals incomplete convergence with penguins (Spheniscidae) due to differing ancestral states

Abstract

Despite longstanding interest in convergent evolution, factors that result in deviations from fully convergent phenotypes remain poorly understood. In birds, the evolution of flightless wing-propelled diving has emerged as a classic example of convergence, having arisen in disparate lineages including penguins (Sphenisciformes) and auks (Pan-Alcidae, Charadriiformes). Nevertheless, little is known about the functional anatomy of the wings of flightless auks because all such taxa are extinct, and their morphology is almost exclusively represented by skeletal remains. Here, in order to re-evaluate the extent of evolutionary convergence among flightless wing-propelled divers, wing muscles and ligaments were reconstructed in two extinct flightless auks, representing independent transitions to flightlessness: Pinguinus impennis (a crown-group alcid), and Mancalla (a stem-group alcid). Extensive anatomical data were gathered from dissections of 12 species of extant charadriiforms and 4 aequornithine waterbirds including a penguin. It was found that the wings of both flightless auk taxa were characterized by an increased mechanical advantage of wing elevator/retractor muscles, and decreased mobility of distal wing joints, both of which are likely advantageous for wing-propelled diving and parallel similar functional specializations in penguins. However, the conformations of individual muscles and ligaments underlying these specializations differ markedly between penguins and flightless auks, instead resembling those in each respective group’s close relatives. Thus, the wings of these flightless wing-propelled divers can be described as convergent as overall functional units, but are incompletely convergent at lower levels of anatomical organization—a result of retaining differing conditions from each group’s respective volant ancestors. Detailed investigations such as this one may indicate that, even in the face of similar functional demands, courses of phenotypic evolution are dictated to an important degree by ancestral starting points.

Incomplete convergence of gliding mammal skeletons*

“…Recent studies have demonstrated that incomplete convergence may be especially common (Losos 2011;Kaeuffer et al 2012;Moen et al 2016), even among "classic" examples of convergence such as flightless birds (Watanabe et al 2020) and hypercarnivores (Meloro et al 2015). Gliders provide further evidence for this conclusion.…”

“…2016), even among “classic” examples of convergence such as flightless birds (Watanabe et al. 2020) and hypercarnivores (Meloro et al. 2015).…”

Convergent evolution in dippers (Aves, Cinclidae): The only wing‐propelled diving songbirds

“…While these changes in flight muscle insertion may be apomorphic in dippers, that changes in muscular insertions occur after an increase in the relative mass of the flight muscles merits further investigation as pattern general to the evolution of WPD. Notable associated myological and osteological differences have been documented between flightless auks and penguins (Smith & Clarke, 2015; Watanabe et al, 2020), but myological comparisons of volant WPD birds remain to be made.…”

“…Characteristics of integument (e.g., feather density, relative length of primaries and rectrices, narial coverings), the relative size of external nares as well as differences in levels of subcutaneous fatty tissues and relative size of integumentary glands were assessed. Special consideration was also given to the primary flight musculature (m. pectoralis and m. supracoracoideus) as both of these muscles provide thrust during WPD (Kozlova, 1961;Watanabe et al, 2020). The following formalin-preserved and skinned specimens were also evaluated: C. mexicanus (USNM 530549, 196710) Early shifts in integument preceding musculoskeletal shifts have been reported in the penguin stem lineage and some shifts in wing feathering even precede loss of flight in waterbirds (Clarke et al, 2010;Wang & Clarke, 2015).…”

“…The following formalin-preserved and skinned specimens were also evaluated: C. mexicanus (USNM 530549, 196710) Early shifts in integument preceding musculoskeletal shifts have been reported in the penguin stem lineage and some shifts in wing feathering even precede loss of flight in waterbirds (Clarke et al, 2010;Wang & Clarke, 2015). Integumentary traits in alcids, penguins, and diving petrels were evaluated from the following sources (Clarke et al, 2010;Kulp et al, 2018;McKitrick, 1991;Schreiweis, 1982;Smith, 2014;Wang & Clarke, 2015;Watanabe et al, 2020). From an osteological perspective, plotopterids closely approach the highly derived features of penguins (e.g., decreased maneuverability of forelimb; Raikow et al, 1988).…”