Evolution of discrete reproductive strategies in Phlox (Polemoniaceae)

Abstract

Fitness is defined as an individual’s relative success in reproduction and survival. As populations adapt to changing ecological and environmental conditions, the fitness landscape can favor divergent reproductive strategies, leading to correlated and cascading effects on reproductive biology. In flowering plants, maternal fitness depends on both seed size—a proxy for offspring quality—and seed number, reflecting offspring quantity. However, a fundamental tradeoff between seed size and number constrains the potential for simultaneous fitness gains in both traits. In this thesis, I use an eco-evo-devo framework to investigate how and why variation in seed number arises within the wildflower genus Phlox. In Chapter 1, I characterize the developmental basis of ovule number variation across five independent origins of a novel multi-ovulate ovule packaging morphology from a single-ovulate ancestral state. We show that a dramatic shift at the earliest stages of development in the allometric relationship between ovule size and ovary size governs the transition from a single-ovulate to a multi-ovulate state. Specifically, this allometric difference reflects two distinct developmental trajectories: one in which a larger ovary yields a larger, single seed and the other in which a larger ovary yields an increased number of smaller seeds. The convergent evolution of this novel developmental response in every instance of the derivation of the multi-ovulate condition may reflect a previously unappreciated constraint on ovule development. Furthermore, this single mechanism appears to be the basis of variation in the size and number of both seeds and ovules. In Chapter 2, I created an F2 hybrid population using crosses between sister species Phlox drummondii and P. roemeriana, representing the extremes of not only ovule packaging strategies but also correlated variation in flower size and number. Most measured traits in the F2 population show unimodal distributions, consistent with a genetic architecture involving multiple loci. Significant correlations between ovary size, ovule number, flower size, and flower number among F2 plants suggest that underlying genetic constraints may shape both the seed size/number and flower size/number tradeoffs, as well as the relationship between them. Finally, in Chapter 3, I characterize a natural polymorphism in Phlox longifolia involving the ancestral single-ovulate strategy and the derived multi-ovulate strategy. I show that environmental variation alone cannot explain the phenotypic differences observed across 102 populations spanning the species' range, suggesting a role of genetic variation. Collectively, these studies reveal the developmental underpinnings and the role of genetic variation—including integration with other phenotypic traits—of seed packaging strategies in Phlox, offering novel insight into how changes in fundamental developmental pathways generate morphological diversity in natural populations and influence key components of the tradeoff between seed size and number.