Coiling directions in the planktonic foraminifer Pulleniatina: A complex eco-evolutionary dynamic spanning millions of years

Abstract

Planktonic foraminifera are heterotrophic sexually reproducing marine protists with an exceptionally complete fossil record that provides unique insights into long-term patterns and processes of evolution. Populations often exhibit strong biases towards either right (dextral) or left (sinistral) shells. Deep-sea sediment cores spanning millions of years reveal that some species show large and often rapid fluctuations in their dominant coiling direction through time. This is useful for biostratigraphic correlation but further work is required to understand the population dynamical processes that drive these fluctuations. Here we address the case of coiling fluctuations in the planktonic foraminifer genus Pulleniatina based on new high-resolution counts from two recently recovered sediment cores from either side of the Indonesian through-flow in the tropical west Pacific and Indian Oceans (International Ocean Discovery Program Sites U1486 and U1483). We use single-specimen stable isotope analyses to show that dextral and sinistral shells from the same sediment samples can show significant differences in both carbon and oxygen isotopes, implying a degree of ecological separation between populations. In one case we detect a significant difference in size between dextral and sinistral specimens. We suggest that major fluctuations in coiling ratio are caused by cryptic populations replacing one another in competitive sweeps, a mode of evolution that is more often associated with asexual organisms than with the classical ‘biological species concept’.

Paleoecology and evolutionary response of planktonic foraminifera to the mid-Pliocene Warm Period and Plio-Pleistocene bipolar ice sheet expansion

“…Another plausible scenario may be the existence of indeterminate cryptic diversity within the D. altispira morphospecies complex where multiple ecological strategies or phylogenetic expressions may be present (e.g., Huber et al, 1997;Bijma et al, 1998;de Vargas et al, 1999de Vargas et al, , 2002Weiner et al, 2012;Schiebel and Hemleben, 2017;Nirmal et al, 2021;Pearson and Penny, 2021), and the stepwise changes observed by Woodhouse et al (2021) may indicate the systematic loss of "cryptic genotypes" within this morphospecies complex. Indeed, Pearson and Penny (2021), hypothesized that dramatic abundance switches in the Indo-Pacific Warm Pool of ecologically distinct, alternately coiled populations of Pulleniatina morphospecies may signify re- placement by distinct cryptic genotypes, and such coiling switches are noted throughout the planktonic foraminiferal fossil record (Ericson et al, 1955;Saito et al, 1975;Bossio et al, 1976;Hallock and Larsen, 1979;Hornibrook, 1982;Scott et al, 1990;Norris and Nishi, 2001;Winter and Pearson, 2001;Crundwell and Nelson, 2007;Wade et al, 2011;Pearson and Ezard, 2014;Crundwell, 2015a, b;Levin et al, 2016;Wallace et al, 2019;Crundwell and Woodhouse, 2022a, b). Therefore, the range of interpreted paleoecologies in D. altispira may, in fact, be due to the occurrence of distinct cryptic populations from across the geological record.…”

“…Their calcareous skeletons, or tests, preserve not only their entire life history, but also a biogeochemical expression of the surrounding water column (e.g., Edgar et al, 2017). These features allow for high-resolution species-specific quantification of physiological and ecological adaptation through periods of climate variability (e.g., Knappertsbusch, 2007;Wade et al, , 2016Hull and Norris, 2009;Wade and Olsson, 2009;Edgar et al, 2013a;Aze et al, 2014;Pearson and Ezard, 2014;Weinkauf et al, 2014Weinkauf et al, , 2019Brombacher et al, 2017aBrombacher et al, , 2021Falzoni et al, 2018;Si and Aubry, 2018;Fox et al, 2020;Todd et al, 2020;Kearns et al, 2021Kearns et al, , 2022Pearson and Penny, 2021;Shaw et al, 2021;Woodhouse et al, 2021;Friesenhagen, 2022;Hupp et al, 2022;Woodhouse and Swain et al, 2023).…”

Biostratigraphic utility of coiling direction in Miocene planktonic foraminiferal genus Paragloborotalia

“…The number of sinistral specimens per sample was then divided by the total number of specimens counted, and then multiplied by 100 to give the percent of sinistral forms. A 95 % confidence interval was added for each sample using the Modified Wald Method (e. g., Agresti and Coull 1998), following the application of this method for producing coiling error bars in Pulleniatina (Pearson and Penny 2021).…”

Taxonomic review of living planktonic foraminifera

“…Instead, we highlight key cases where names that must be rejected for extant taxa may be retained when classifying fossil species. This problem is illustrated by cases like the usage in fossil and extant material of Trilobatus trilobus and T. sacculifer (Spezzaferri et al, 2015) or the nature of the fossil taxon Pulleniatina finalis, which describes a morphology that ranges to the present, but whose existence as a biological taxon cannot be substantiated (Pearson and Penny, 2021).…”