Origin of division of labor is decoupled from polymorphism in colonial animals

Abstract

Division of labor, the specialization of sometimes phenotypically divergent cell types or group members, is often associated with ecological success in eukaryotic colonial organisms. Despite its many independent evolutionary origins, how division of labor emerges remains unclear. Conventional hypotheses tend toward an "economic" model, so that biological division of labor may reflect a partitioning of preexisting tasks and morphologies into specialized colony members. Here, we present an alternative model of the origin of division of labor, which can explain the evolution of new functions within a colony. We show that in colonies of the Cretaceous aged (103-96 Ma) fossil bryozoan of the genus Wilbertopora, the first cheilostome bryozoan to evolve polymorphism, preexisting morphologies were not simply partitioned among new members, but instead expanded into novel morphospace as they lost functions, specifically feeding. This expansion occurred primarily during two pulses of heightened morphological disparity, suggesting that the evolution of polymorphism corresponded to relaxed constraints on morphology and perhaps to the exploration of novel functions. Using a simple model of physiological connections, we show that regardless of the functionality of these new colony members, all nonfeeding members could have been supported by neighboring feeding members. This suggests that geometric constraints and physiological connectedness could be prerequisites for evolving both polymorphism and division of labor in modular organisms, and that a classic partitioning model of specialization cannot be broadly applied to biological systems.

Fig. 1.

A) Two potential patterns of phenotypic and functional evolution in colonial organisms. In the case of Wilbertopora, squares labeled with “Az” represent the ancestral body type (autozooids); squares labeled with “Av” represent the novel polymorph (avicularia). In the partitioning scenario, avicularia evolve through the partitioning of preexisting functions and variation in Wilbertopora. The range of autozooid functions and morphologies decreases as avicularia take on particular functions that used to be performed by autozooids. The total amount of variation in a colony remains similar to that of the ancestral state, but this variation becomes split between autozooids and avicularia. In the expansion scenario, avicularia evolve as an extension of autozooidal variation, expanding the range of variation in a colony. Avicularia then lose autozooid functions and become adapted to completely new functions in the colony. B) Polymorphs within two Cretaceous species of Wilbertopora. Wilbertopora listokinae, Cheetham et al. (22) (USNM PAL 216175), showing an autozooid (az) and avicularium (av) with ovicells (ov). Wilbertopora acuminata, Cheetham et al. (USNM PAL 216143).

Fig. 2.

Morphological evolution of polymorph shape (as outlines of a zooid's orifice and opesia, which together comprise the frontal area of a zooid) in colonies of Wilbertopora. A) Morphospace of polymorphs defined by first two principal components (PCs). Each point represents a single zooid. B) Difference in mean shapes of autozooids and avicularia within colonies. Points and bars show mean and SD of values, respectively, within time intervals. C) Shape disparity of autozooids and avicularia within colonies; solid points with bars show mean and SD among colonies per time interval. Time slices show the midpoint of stratigraphic formations, but their relative spacing is uniform for visualization purposes.

Fig. 3.

Mean-centered and scaled (Z-scores) divergence of autozooidal and avicularian morphologies compared to avicularian disparity within colonies over time. The time series progresses from time t₁ to t₉, with each labeled point representing a subsequent formation in the Washita group (see midpoints of time intervals in Fig. 2). The intervals with high avicularian disparity tend to precede intervals with high divergence between autozooids and avicularia within colonies.

Fig. 4.

Comparing A) divergence, B) disparity, and C) ovicell frequency between Wilbertopora colonies with and without avicularian ovicells. Points show the mean value, thick line segments show standard deviation (SD), and thin line segments show the range of values. Divergence is significantly different between groups (Table S7, P < 0.01), disparity is marginally different between groups (Table S8, P ∼ 0.1), and ovicell frequency is significantly different between groups (Table S9, P < 0.01). Results here show colonies with more than 30 zooids and have at least one ovicell.

Fig. 5.

Bryozoan colonies vary in growth form and therefore in their network of physiological connections. Growth forms illustrated for A) the uniserial Rhammatopora (PI BZ 8149) and B) multiserial Wilbertopora (USNMPAL 186572). The different budding geometries of each genus lead to different ratios of feeding zooids to growing-edge zooids. Autozooids (feeding zooids) are denoted with “Az” and avicularia (non-feeding zooids) are denoted with “Av”. C) The supply/demand ratio within a colony is a function of the number of feeding zooids and the number of newly budded zooids. Multiserial growth, exhibited in Wilbertopora, generates a smaller energy surplus than uniserial growth, indicating higher colony efficiency. The presence of more nonfeeding polymorphs reduces the energy surplus in colonies and works to equilibrate energetic supply with demand. D) An example of an incidence matrix showing physiological connections for a colony of Wilbertopora. Zooids with red labels in B and D are nonfeeding avicularia, zooids with black labels denote feeding autozooids. The funicular system allows the transport of nutrients between zooids. Feeding zooids can transport nutrients between each other, but nonfeeding avicularia only receive nutrients from neighbors. Arrows indicate directions of energy exchange. We model diffusion of nutrients along the graph of the colony to evaluate if the colony can support extra nonfeeding zooids. We find that adding polymorphic nonfeeders within a colony increases the E) total colony flux of energy and F) average per zooid energy benefit increases with the presence of nonfeeding zooids and their divergence. The contemporaneous genus Rhammatopora only has feeding zooids and is plotted as a point of comparison.