Functional innovation through vestigialization in a modular marine invertebrate

Abstract

Few studies show how morphological vestigialization may facilitate functional innovation. Fewer still describe the co-occurrence of the derived and more ancestral structures in the same genetic individual. In the present study, we explore that rare instance in a modular (colonial) marine invertebrate. Using laser scanning confocal microscopy with fluorescent staining and behavioural observations, we describe homologous structures in polymorphic modules (zooids) in the bryozoan Bugula flabellata and document the occurrence of previously unreported retractor and circular muscles in the more derived module, the bird's-head avicularium. In the evolution of a sessile feeding zooid to a moveable nonfeeding zooid with sensory and grasping functions, transformations were effected in the food-capture apparatus, orificial structures, musculature, and sensory structures. We expand on and clarify previous reports of homologies between ancestral and derived modules in bryozoans and argue that vestigialization and augmentation of homologous structures were coincident with functional innovations in the avicularium. The present study offers rare evidence for the evolution of functional innovation through vestigialization.

Phylogeny and diversification of bryozoans

“…These characters include the following: calcified frontal shields; polymorphic zooids (avicularia), with mandibles (hypertrophied homologues of autozooidal opercula) that can snap shut to trap predators (Carter et al . ; Lidgard et al . ); and vibracula, a highly modified type of avicularium with a whip‐like seta carrying out sweeping movement to deter predators and epizoites (Lidgard et al .…”

Differential Gene Expression Between Polymorphic Zooids of the Marine BryozoanBugulina stolonifera

“…All polymorphic zooids are incapable of feeding and instead, obtain nutrients from the funicular system, a tissue extension which interconnects all zooids via pores in zooecium walls in gymnolaemates, one of the three major bryozoan clades, which contains the order Cheilostomata (Mukai et al 1997;Carter et al 2010b;Schwaha et al 2020). One of the most commonly observed polymorphic zooids found in cheilostome colonies is the avicularium, a derived module that is homologous to the feeding autozooid (Carter et al 2011).…”

“…Instead, they must obtain nutrients from neighboring autozooids via the funicular system (Mukai et al 1997). Although morphologically diverse, most avicularia are characterized by having an enlarged, hinged operculum-derived "mandible" that can be opened and shut with pairs of hypertrophied muscles (Winston 1984;Carter et al 2011;Schack et al 2019).…”

“…All polymorphic zooids are incapable of feeding and instead, obtain nutrients from the funicular system, a tissue extension which interconnects all zooids via pores in zooecium walls in gymnolaemates, one of the three major bryozoan clades, which contains the order Cheilostomata ( Mukai et al 1997 ; Carter et al 2010b ; Schwaha et al 2020 ). One of the most commonly observed polymorphic zooids found in cheilostome colonies is the avicularium, a derived module that is homologous to the feeding autozooid ( Carter et al 2011 ). Avicularia have often been presumed to be defensive, as avicularia of certain species have been observed trapping micro predators ( Kaufmann 1968 ; Winston 1986 , 1991 ), however empirical evidence supporting this hypothesis in most bryozoan species is largely lacking ( Winston 1984 ; Carter et al 2010a ).…”

“…Although they possess vestiges of a polypide, avicularia are incapable of feeding ( Hyman 1959 ; Silén 1977 ; Carter et al 2010b 2011 ). Instead, they must obtain nutrients from neighboring autozooids via the funicular system ( Mukai et al 1997 ).…”