Turbulent adaptive landscape shaped size evolution in modern ocean giants

Abstract

Adaptive landscapes are central to evolutionary theory, forming a conceptual bridge between micro- and macro-evolution. 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 timescales. Constant shifts in selection pressures mean the peaks themselves also evolve through time, 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 approx. 53 million year evolutionary history, using 345 living and fossil taxa. We analyse shifts in long-term mean size and directional changes in average trait values 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 taxa, 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.

Innovation and elaboration on the avian tree of life

“…However, individual species-level variation in the past could also have led to a shift in a clade's line of least evolutionary resistance through different evolutionary routes on a dynamic adaptive landscape. Taken together, our results suggest that the signature of evolutionary reorientations in deep-time (innovation), coupled with elaboration at the species-level, is a robust explanation of the massive diversity of bird beaks we observe today and is consistent with recent suggestions that apparently abrupt phenotypic shifts observed in univariate analyses can be explained by gradual Darwinian processes [2,3,16]. Indeed, the global phylogenetic major axis of phenotypic variation is an emergent property of reorientation of trait space among clades that requires no special evolutionary process: megaevolutionary patterns appear to be an inevitable outcome of evolution on a shifting adaptive landscape.…”

“…Recent evidence suggests that this stability can even extend over macroevolutionary timescales spanning tens of millions of years [10]. However, while the evolutionary line of genetic least resistance explicitly reflects genetic constraints, the macroevolutionary major axis of phenotypic variation is an emergent property of genomic and developmental constraints interacting with selection on a moving adaptive landscape [3, 12]. The widespread evidence of major shifts in phenotypes across the tree of life [1, 2, 13, 14, 15, 16] suggests a conflict in the direction of phenotypic evolution across scales where macroevolutionary divergence away from the major axis of phenotypic variation results in megaevolutionary divergence leading to distinct phenotypes and/or directions of evolution.…”

“…A long-standing proposal is that most morphological diversity at a macroevolutionary scale (among species) arises along a microevolutionary “line of least resistance”. However, we frequently observe major shifts in phenotypes among lineages [1, 2, 3], suggesting that species or clades may also evolve away from the line of least resistance [4]. At the macroevolutionary scale, evolution along a common major axis has been termed elaboration whereas evolution away from that major axis is termed innovation [5].…”