Discovery of a sensory organ that coordinates lunge feeding in rorqual whales

Abstract

Top ocean predators have evolved multiple solutions to the challenges of feeding in the water1, 2, 3. At the largest scale, rorqual whales (Balaenopteridae) engulf and filter prey-laden water by lunge feeding4, a strategy that is unique among vertebrates1. Lunge feeding is facilitated by several morphological specializations, including bilaterally separate jaws that loosely articulate with the skull5, 6, hyper-expandable throat pleats, or ventral groove blubber7, and a rigid y-shaped fibrocartilage structure branching from the chin into the ventral groove blubber8. The linkages and functional coordination among these features, however, remain poorly understood. Here we report the discovery of a sensory organ embedded within the fibrous symphysis between the unfused jaws that is present in several rorqual species, at both fetal and adult stages. Vascular and nervous tissue derived from the ancestral, anterior-most tooth socket insert into this organ, which contains connective tissue and papillae suspended in a gel-like matrix. These papillae show the hallmarks of a mechanoreceptor, containing nerves and encapsulated nerve termini. Histological, anatomical and kinematic evidence indicate that this sensory organ responds to both the dynamic rotation of the jaws during mouth opening and closure, and ventral groove blubber7 expansion through direct mechanical linkage with the y-shaped fibrocartilage structure. Along with vibrissae on the chin9, providing tactile prey sensation, this organ provides the necessary input to the brain for coordinating the initiation, modulation and end stages of engulfment, a paradigm that is consistent with unsteady hydrodynamic models and tag data from lunge-feeding rorquals10, 11, 12, 13. Despite the antiquity of unfused jaws in baleen whales since the late Oligocene14 (~23 28 million years ago), this organ represents an evolutionary novelty for rorquals, based on its absence in all other lineages of extant baleen whales. This innovation has a fundamental role in one of the most extreme feeding methods in aquatic vertebrates, which facilitated the evolution of the largest vertebrates ever.