Turbulent adaptive landscape shaped size evolution in modern ocean giants

Abstract

ABSTRACTAdaptive landscapes are central to evolutionary theory, forming a conceptual bridge between micro- and macro-evolution1–4. Evolution by natural selection across an adaptive landscape should drive lineages towards fitness peaks, shaping the distribution of phenotypic variation within and among clades over evolutionary timescales5. Constant shifts in selection pressures mean the peaks themselves also evolve through time4, thus a key challenge is to identify these ‘ghosts of selection past’. Here, we characterise the global and local adaptive landscape for total length in cetaceans (whales and dolphins) across their ~ 53 million year evolutionary history, using 345 living and fossil taxa. We analyse shifts in long-term mean size6 and directional changes in average trait values7 using cutting-edge phylogenetic comparative methods. We demonstrate that the global macroevolutionary adaptive landscape of cetacean body size is relatively flat, with very few peak shifts after cetaceans colonised the oceans. Local peaks represent trends along branches linked to specific adaptations such as deep diving. These results contrast with previous studies using only extant taxa8, highlighting the vital role of fossil data for understanding macroevolutionary dynamics. Our results indicate that adaptive peaks are constantly changing and are associated with subzones of local adaptations, resembling turbulent waters with waves and ripples, creating moving targets for species adaptation. In addition, we identify limits in our ability to detect some evolutionary patterns and processes, and suggest multiple approaches are required to characterise complex hierarchical patterns of adaptation in deep-time.