Trait–fitness associations do not predict within-species phenotypic evolution over 2 million years

Long-term patterns of phenotypic change are the cumulative results of tens

of thousands to millions of years of evolution. Yet, empirical and theoretical

studies of phenotypic selection are largely based on contemporary populations.

The challenges in studying phenotypic evolution, in particular

trait–fitness associations in the deep past, are barriers to linking microand

macroevolution. Here, we capitalize on the unique opportunity offered

by a marine colonial organism commonly preserved in the fossil record to

investigate trait–fitness associations over 2 Myr. We use the density of

female polymorphs in colonies of Antarctothoa tongima as a proxy for fecundity,

a fitness component, and investigate multivariate signals of trait–fitness

associations in six time intervals on the backdrop of Pleistocene climatic

shifts. We detect negative trait–fitness associations for feeding polymorph

(autozooid) sizes, positive associations for autozooid shape but no particular

relationship between fecundity and brood chamber size. In addition,

we demonstrate that long-term trait patterns are explained by palaeoclimate

(as approximated by ∂¹⁸O), and to a lesser extent by ecological interactions

(i.e. overgrowth competition and substrate crowding). Our analyses show

that macroevolutionary outcomes of trait evolution are not a simple

scaling-up from the trait–fitness associations.