Rare but persistent asexual reproduction explains the success of planktonic foraminifera in polar oceans

Abstract

The reproductive strategy of planktonic foraminifera, key pelagic calcifiers, has long remained elusive, hampering efforts to understand and model their population dynamics. This is particularly critical in polar oceans where their success relies on rapid population growth after the polar night. Here, we provide field and laboratory observations constraining the reproductive cycle of the dominant polar species Neogloboquadrina pachyderma in Antarctic and Arctic waters. We observe that asexual reproduction is a rare but persistent element of the reproductive strategy and that it is reflected in a dimorphism in proloculus and in the ratio of shell size versus the number of chambers between sexually and asexually produced individuals. This dimorphism in natural populations reveals that asexual reproduction supplies more than 75% of adult individuals. This indicates a multigenerational reproduction strategy, where the majority of the population releases gametes to facilitate recombination, while a minority persistently reproduces asexually, allowing rapid population growth as a prerequisite for success in the polar oceans.

Continuous reproduction of planktonic foraminifera in laboratory culture

“…All specimens that reproduced via multiple fission in this study shared the specific traits described in the method section among which are very thin and translucent shell walls, in contrast to the often observed encrusted shells previously reported to be associated to gametogenesis in Neogloboquadrinids (e.g. Davis et al, 2017;Meilland et al, 2023). Indeed, in previous culture work on N. pachyderma we observed a clear thickening of specimens' shell walls before gamete release and obtained what could be referred to as encrusted shells while being in stable culture conditions and thus, irrespective of a change in depth or environmental conditions (Meilland et al, 2023;WestgÅrd et al, 2023).…”

“…Anderson & Bé, 1976;Erez et al, 1991) followed by karyogamy (thus far unobserved), assuming obligate outbreeding because autogamy has never been documented. Multiple fission (often referred to as "asexual reproduction" in foraminifera literature) was recently observed in different groups of planktonic foraminifera (Neogloboquadrina pachyderma, Kimoto and Tsuchiya (2006), Davis et al (2020), Meilland et al (2023); Globigerinita uvula, Takagi et al (2020)) and confirms that like their benthic ancestors, planktonic foraminifera life cycles probably have a biphasic basis (Darling et al, 2023).…”

“…Our study suggests that even if only a small portion of planktonic foraminifera reproduce via multiple fission in the natural population (Meilland et al, 2023) it is possible, using specific morphologic traits, to increase its occurrence in the laboratory to a level that one can obtain thousands of offspring from only a hundred specimens picked from plankton material. The existence of these indicative morphologic traits suggests that the determination of whether specimens of N. pachyderma will reproduce sexually or via multiple fission occurs early in its life.…”

“…At stations 25,209 and 25,210, higher concentrations of N. pachyderma were found, allowing us to select a total of 120 specimens based on the presence of intense red cytoplasm in all chambers, their small size, and the high sphericity of their individual chambers and the thinness and transparency of the overall shell. These traits had been identified in the shells of the specimens that had reproduced via multiple fission in Meilland et al (2023). These specimens will be referred to as the "selectively picked" in the manuscript.…”

Environmental Controls of Size Distribution of Modern Planktonic Foraminifera in the Tropical Indian Ocean

“…Nevertheless, in a study investigating the distribution of planktonic foraminifera in the Arctic Ocean, Carstens et al (1997) reported a weak bimodal SFD in N. pachyderma populations (n = 6,768). Planktonic foraminiferal SFD can be controlled by multiple processes including surface water physical and chemical properties (Naidu & Malmgren, 1995), reproductive cycle (Bijma et al, 1994), size-dependent weight, morphology (spinose vs. non-spinose) and sinking speed (Bijma et al, 1994;Takahashi & Be, 1984), dissolution (Peeters et al, 1999), cryptic diversity (Huber et al, 1997), winnowing after settling on the sea floor (Peeters et al, 1999), and the tendency for the morphological characteristics of a species to vary depending on how the species reproduces (that is, sexually or asexually) (Meilland et al, 2022). Since no published water column size spectra are available to the best of our knowledge to compare our data set with living communities, we infer that the SFDs of the well-represented species reported here are representative of their regional SFDs.…”