An extinction event in planktonic Foraminifera preceded by stabilizing selection

Abstract

Unless they adapt, populations facing persistent stress are threatened by extinction. Theoretically, populations facing stress can react by either disruption (increasing trait variation and potentially generating new traits) or stabilization (decreasing trait variation). In the short term, stabilization is more economical, because it quickly transfers a large part of the population closer to a new ecological optimum. However, stabilization is deleterious in the face of persistently increasing stress, because it reduces variability and thus decreases the ability to react to further changes. Understanding how natural populations react to intensifying stress reaching terminal levels is key to assessing their resilience to environmental change such as that caused by global warming. Because extinctions are hard to predict, observational data on the adaptation of populations facing extinction are rare. Here, we make use of the glacial salinity rise in the Red Sea as a natural experiment allowing us to analyse the reaction of planktonic Foraminifera to stress escalation in the geological past. We analyse morphological trait state and variation in two species across a salinity rise leading to their local extinction. Trilobatus sacculifer reacted by stabilization in shape and size, detectable several thousand years prior to extinction. Orbulina universa reacted by trait divergence, but each of the two divergent populations remained stable or reacted by further stabilization. These observations indicate that the default reaction of the studied Foraminifera is stabilization, and that stress escalation did not lead to the emergence of adapted forms. An inherent inability to breach the global adaptive threshold would explain why communities of Foraminifera and other marine protists reacted to Quaternary climate change by tracking their zonally shifting environments. It also means that populations of marine plankton species adapted to response by migration will be at risk of extinction when exposed to stress outside of the adaptive range.

Fig 1. Summary of the sampling material from piston core Geo-TÜ KL09.

(a) Map of the sampling area with indication of the core position. (b) Stratigraphic plot with core image. Accumulation rates, relative abundances in relation to other species of planktonic Foraminifera, and the incidence of abnormal morphotypes in Orbulina universa and sacculifer-morphotypes in Trilobatus sacculifer is indicated (shaded area depicts 95% confidence intervals). The aplanktonic zone begins at approximately 438 kyrs BP. The two intervals of dropping abundance for O. universa (Intervals 1 and 2) and the three phases defined for T. sacculifer (Phases 1–3) based on relative abundances are indicated. The δ¹⁸O_{G. ruber} measurements and the three-point moving average relative sea level in the Red Sea [26] is also shown. Example scanning electron microscope images of the two investigated species are shown in the respective panels. The O. universa specimen was cracked open to reveal the juvenile shell inside. Image of T. sacculifer from Hesemann [33].

Fig 2. Morphology of Orbulina universa from marine isotope stage 12 in the Red Sea.

(a) Shell size is showing bimodality after 445.4 kyrs BP, when a small population slowly appeared. (b) The variation in shell size is larger in the large population but generally decreased over time. (c) Shell roundness is rather stable in the large population, and considerably lower in the small population. (d) The variation in shell roundness is considerably higher in the small population but decreased slightly in the larger population toward local extinction. Raw values are plotted as grey dots, mean values as lines, and 95% confidence intervals as shaded areas. The intervals based on species abundance (compare Fig 1) are indicated.

Fig 3. Morphology of Trilobatus sacculifer from marine isotope stage 12 in the Red Sea.

The three phases defined by abundance (compare Fig 1) are indicated. (a) Shell size and its variation decrease toward the local extinction (compare S1 File). Raw values (grey dots) are plotted alongside the sample mean and coefficient of variation (solid lines) and their 95% confidence intervals (shaded area). (b) Shell shape (Riemannian shape distance from the mean shape) excluding sacculifer-morphotypes (compare S1 File). Raw values (grey dots) are plotted alongside the sample mean and standard deviation (solid lines) including the 95% confidence interval (shaded area).

Fig 4. Stabilizing selection in planktonic Foraminifera during marine isotope stage 12 in the Red Sea.

(a–b) The variation of shell size and shell roundness (including 95% confidence interval) in the incumbent population of Orbulina universa decreased toward local extinction. The small population had an inherently reduced size variation but higher variation of shell roundness. (c) The shape variation (Riemannian shape distance from the mean shape, excluding sacculifer-morphotype) in Trilobatus sacculifer decreased significantly toward the local extinction (Phase 3, compare Fig 1). Error bars depict the 95% confidence interval. (d) Canonical variates analysis (CVA) of the shape of T. sacculifer (excluding sacculifer-morphotype). Points indicate specimens, ellipses indicate the 95% confidence interval of the standard deviation on the centroid, black silhouettes depict the morphology at the extremal points of the canonical variate (CV) 1 and 2 axes, respectively.