The Breakdown of Static and Evolutionary Allometries during Climatic Upheaval

Abstract

15The influence of within-species variation and covariation on evolutionary patterns is 16 well established for generational and macroevolutionary processes, most prominently 17 through genetic lines of least resistance. However, it is not known whether intraspecific 18 phenotypic variation also directs microevolutionary trajectories into the long term 19 when a species is subject to varying environmental conditions. Here we present a 20 continuous, high-resolution bivariate record of size and shape changes among 12,633 21 individual planktonic foraminifera of a surviving and an extinct-going species over 500 22 thousand years. This time interval spans the late Pliocene to earliest Pleistocene 23 intensification of Northern Hemisphere glaciation, an interval of profound climate 24 upheaval that can be divided into three phases of increasing glacial intensity. We found 25 that within each of these three Plio-Pleistocene climate phases the within-population 26 allometries predict evolutionary change from one time-step to the next, and that the 27 2 within-phase among-population (i.e. evolutionary) allometries match their 28 corresponding static (within-population) allometries. However, the evolutionary 29 allometry across the three climate phases deviates significantly from the static and 30 phase-specific evolutionary allometries in the extinct-going species. Although 31 intraspecific variation leaves a clear signature on mean evolutionary change from one 32 time-step to the next, our study suggests that the link between intraspecific variation 33 and longer-term micro-and macroevolutionary phenomena is prone to environmental 34 perturbation that can overcome constraints induced by within-species trait covariation. 35 36 3 Introduction 37

Assessing adequacy of models of phyletic evolution in the fossil record

“…This changed when Hunt (Hunt, , ; Hunt, Bell, & Travis, ; Hunt, Hopkins, & Lidgard, ; Hunt, Wicaksono, Brown, & Macleod, ) developed a model framework that allowed an objective evaluation of relative fit of different models to fossil time series based on their AIC scores. Hunt's models of the canonical modes stasis, directional change and random walk are widely used when analysing phyletic time series and his model framework has greatly advanced our ability to interpret the fossil record (e.g., Brombacher, Wilson, Bailey, & Ezard, ; Hopkins & Lidgard, ; Hunt, ; Hunt et al., ; Pearson & Ezard, ; Spanbauer, Fritz, & Baker, ; Voje, ).…”

Developmental bias, macroevolution, and the fossil record

“…At the species level, the fine structure of phenotypic (co) variation seems to be fairly labile. It can change rapidly in response to directional selection, even in natural populations (e.g., Assis, Patton, Hubbe, & Marroig, 2016); the variation signal in fossil ostracods fades over a few million years (Hunt, 2007), with a similar timeframe reported by Schluter (1996) from estimated divergence times for extant taxa; it is disrupted in planktic foraminifera by climate shifts (Brombacher, Wilson, Bailey, & Ezard, 2017); and static allometry-that is intraspecific variation among adults-while stable within species generally does not seem to persist among related species (Voje, Hansen, Egset, Bolstad, & Pélabon, 2014). At higher levels within larger clades, the direction and eccentricity of larger-scale multivariate variation is stable -and predictive of evolutionary patterns-within ungulate families and bird clades but differs among them (Haber, 2016;Watanabe, 2018).…”

“…Thus, alternative mechanisms must also be considered, including release from interactions with pterosaurs, nonavian dinosaurs, and Mesozoic bird lineages outside the crown, all of which were lost at the end of the Mesozoic Era. For example, in Plio-Pleistocene planktic foraminifera, evolutionary changes tend to be aligned with allometric patterns, but shifts in climate state drive clades in different directions (Brombacher et al, 2017). An intermediate, intuitively appealing, possibility is that the loosening and later tightening of developmental bias occurs only at the origin of clades that are founded via an evolutionary novelty sensu G. P. Wagner (2014), that is a trait lacking homology in the ancestor, or radically and irreversibly altered from the ancestral state.…”

Extinctions in marine plankton preceded by stabilizing selection

“…In contrast to comparable cases where fossil material is used (e.g. Weinkauf et al 2014, Brombacher et al 2017), we are here in the unique situation that the extinction events can nearly exclusively be linked to salinity increase (Rohling et al 2009), allowing a qualification of the stressor which acted on the assemblage.…”

“…Understanding the morphological reaction of Foraminifera toward environmental stress could serve as a proxy for environmental reconstructions and further our understanding of evolvability of this organismal group. Past studies have shown that morphological deviations in benthic and planktonic Foraminifera can be caused by environmental forcing (Malmgren and Kennett 1976, Malmgren 1984, Baumfalk et al 1987, Mary and Knappertsbusch 2013, Moller et al 2013, Weinkauf et al 2014, Knappertsbusch 2016, Brombacher et al 2017. But since these studies quantified morphology in very different ways, the results obtained are scarce and controversial.…”