A fly in a tube: Macroevolutionary expectations for integrated phenotypes

Abstract

Phenotypic integration and modularity are ubiquitous features of complex organisms, describing the magnitude and pattern of relationships among biological traits. A key prediction is that these relationships, reflecting genetic, developmental, and functional interactions, shape evolutionary processes by governing evolvability and constraint. Over the last 60 years, a rich literature of research has quantified patterns of integration and modularity across a variety of clades and systems. Only recently has it become possible to contextualize these findings in a phylogenetic framework to understand how trait integration interacts with evolutionary tempo and mode. Here, we review the state of macroevolutionary studies of integration and modularity, synthesizing empirical and theoretical work into a conceptual framework for predicting the effects of integration on evolutionary rate and disparity: a fly in a tube. While magnitude of integration is expected to influence the potential for phenotypic variation to be produced and maintained, thus defining the shape and size of a tube in morphospace, evolutionary rate, or the speed at which a fly moves around the tube, is not necessarily controlled by trait interactions. Finally, we demonstrate this reduced disparity relative to the Brownian expectation for a given rate of evolution with an empirical example: the avian cranium.

Understanding the effect of competition during evolutionary radiations: an integrated model of phenotypic and species diversification

“…In particular, rates of trait evolution can remain constant (or even increase) despite decreasing diversification rates. And in adaptive radiations that reached ecomorphological limits, rates of trait evolution can remain constant despite disparity reaching a plateau, similarly to the ‘fly in a tube’ effect (Felice et al ). These two decoupling are both linked to the continuous reoccupation of vacated trait space after extinctions.…”

Signal evolution and morphological complexity in hummingbirds (Aves:Trochilidae)

“…Morphological disparity measures the range of potential phenotypes a clade can occupy (Hughes et al 2013) and is affected both by rates of and constraints on trait evolution (Felice et al 2018). Under a Brownian motion (BM) model of trait evolution, species trait values "spread out" as a function of time, resulting in a monotonic increase in the amount of variation over time.…”

Measuring the magnitude of morphological integration: The effect of differences in morphometric representations and the inclusion of size

“…; Felice et al. , but see Schluter ). Conversely, lower magnitudes of morphological integration might indicate relative independence between the traits, allowing different aspects of the phenotype to evolve without interference imposed by other parts of the organism.…”

“…A high magnitude of morphological integration means that the available variation is restricted to relatively few dimensions in phenotypic space. In these cases, evolutionary change will be strongly influenced by the interaction between selection and available variation, and we expect evolutionary change to proceed preferentially along these few dimensions in which variation is available (Felsenstein 1988;Goswami et al 2014;Melo et al 2016;Felice et al 2018, but see Schluter 1996). Conversely, lower magnitudes of morphological integration might indicate relative independence between the traits, allowing different aspects of the phenotype to evolve without interference imposed by other parts of the organism.…”