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.

Here, we capitalize on the unique opportunity offered by the polymorphic, colonial nature of a marine organism, the cheilostome bryozoan Antartothoa tongima, commonly preserved in the Pleistocene of the Wanganui Basin (North Island, New Zealand), to estimate trait-fitness associations in the fossil record.

We use the density of female polymorphs as a proxy for fecundity, a fitness component, and investigate multivariate signals of trait-fitness associations for three phenotypic traits, i.e. feeding polymorph size and shape and brood chamber size, in six time intervals of the Pleistocene. We also explored if each of these traits and fecundity are detectably influenced by ecological interactions and climatic shifts.

We found that: (i) the three phenotypic traits and estimates of fitness show substantial variation within and across time intervals, contradicting the apparent phenotypic stasis often observed in the fossil record; (ii) trait-fitness associations are relatively stable on geological time scales; (iii) although “small is fit” within bouts of time presented, “smaller and smaller” was not the resulting phenotypic pattern; (iv) changing paleoclimatic conditions (as approximated by ∂¹⁸O) significantly effects phenotypic traits and fecundity; (v) ecological interactions have only a weak effect.

Our analyses show nuances in the dynamics of trait evolution given changing environmental and ecological conditions over geological time scales. While previous studies investigate life history traits and pioneered quantitative genetics using fossil organisms, this is the first attempt at quantifying trait-fitness associations and understanding how they align with long-term phenotypic evolution. These results will open doors to integrating insights from the fossil record with microevolutionary theory to further bridge empirical and conceptual gaps between micro- and macroevolution.