The origin and diversification of pteropods precede past perturbations in the Earth’s carbon cycle

Abstract

Pteropods are a group of planktonic gastropods that are widely regarded as biological indicators for assessing the impacts of ocean acidification. Their aragonitic shells are highly sensitive to acute changes in ocean chemistry. However, to gain insight into their potential to adapt to current climate change, we need to accurately reconstruct their evolutionary history and assess their responses to past changes in the Earth’s carbon cycle. Here, we resolve the phylogeny and timing of pteropod evolution with a phylogenomic dataset (2,654 genes) incorporating new data for 21 pteropod species and revised fossil evidence. In agreement with traditional taxonomy, we recovered molecular support for a division between “sea butterflies” (Thecosomata; mucus-web feeders) and “sea angels” (Gymnosomata; active predators). Molecular dating demonstrated that these two lineages diverged in the early Cretaceous, and that all main pteropod clades, including shelled, partially-shelled, and unshelled groups, diverged in the mid- to late Cretaceous. Hence, these clades originated prior to and subsequently survived major global change events, including the Paleocene–Eocene Thermal Maximum (PETM), the closest analog to modern-day ocean acidification and warming. Our findings indicate that planktonic aragonitic calcifiers have shown resilience to perturbations in the Earth’s carbon cycle over evolutionary timescales.

Oceanic dispersal barriers in a holoplanktonic gastropod

“…Second, unlike most holoplanktonic animals, they have shells, which provide a record of the ecology and life history of an individual that can be easily measured. Third, pteropods are the only living planktonic animals with a good fossil record (Janssen & Peijnenburg, 2017; Peijnenburg et al, 2020), which allows for comparisons of morphological diversity in extant as well as extinct species and populations. We demonstrated significant spatial population structuring across and within ocean basins in L. bulimoides , a presumably circumglobal species.…”

Toward a global reference database of COI barcodes for marine zooplankton

“…They are thus considered to be vulnerable to ocean acidification, but the deposition of their shells in marine sediments has also provided a unique and invaluable fossil record of the biodiversity of pelagic ecosystems. The fossil record makes these holoplanktonic gastropods particularly useful for studying evolutionary processes in metazoan plankton in the global ocean (Peijnenburg et al 2020;Wall-Palmer et al 2020).…”

The impacts of past, present and future ocean chemistry on predatory planktonic snails

“…Our results demonstrate that the effects of OA on atlantid calcification are not straight forward, and likely depend on whether these organisms are able to survive and maintain calcification under stressful conditions in the long term. Evidence suggests that both shelled pteropods and atlantids survived the Cretaceous-Paleogene extinction event (KPg or KT) and Paleocene-Eocene thermal maximum (PETM), both periods of extreme perturbation in the ocean's carbon cycle [38,39]. These findings give some hope that aragonite shelled holoplanktonic gastropods will be able to adapt to our changing oceans, even though the rate of change is unprecedented relative to the geological record.…”

“…Third, atlantids can have high abundances in cold, mid-high latitude regions that have a higher capacity to absorb atmospheric CO 2 , thus more rapidly becoming acidic compared to warmer regions [26,33]. Yet, despite the supposed vulnerability of aragonite shelled planktonic gastropods to OA, recent research suggests that atlantids and shelled pteropods survived past large-scale global change crises [38,39]. One of these events, the Paleocene-Eocene Thermal Maximum (PETM), is the most analogous geological event to the current Anthropogene climate crisis [40].…”