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 micro- and 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 Antartothoa 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 ∂ 18 O), 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.