An emerging paradigm for the origin and evolution of shelled amoebae, integrating advances from molecular phylogenetics, morphology and paleontology

Abstract

The phylogenetic paradigm of eukaryotic evolution has changed dramatically over the past two decades, with profound reflections on the understanding of life on earth. Arcellinida testate (shelled) amoebae lineages represent some of the oldest fossils of eukaryotes, and the elucidation of their phylogenetic relationships opened a window to the distant past, with important implications for understanding the evolution of life on earth. This four-part essay summarises advances made in the past 20 years regarding: (i) the phylogenetic relationships among amoebae with shells evolving in concert with the advances made in the phylogeny of eukaryotes; (ii) paleobiological studies unraveling the biological affinities of Neoproterozoic vase-shaped microfossils (VSMs); (iii) the interwoven interpretation of these different sets of data concluding that the Neoproterozoic contains a surprising diversity of organisms, in turn demanding a reinterpretation of the most profound events we know in the history of eukaryotes, and; (iv) a synthesis of the current knowledge about the evolution of Arcellinida, together with the possibilities and pitfalls of their interpretation.

Shallow-marine testate amoebae with internal structures from the Lower Devonian of China

“… 13 Recent advances in molecular phylogeny and microbial paleobiology of testate amoebae raise a scenario that, within Arcellinida lineages, the marine-freshwater transition probably occurred multiple times and only during the Phanerozoic. 49 That arcellinids occurred in both the freshwater and shallow-marine environments in the Early Devonian concurs with the very possibility proposed by Lahr, 49 although more fossil evidence is required to provide details and testify for such evolutionary history of Arcellinida.

Figure 4 Palaeoecosystem reconstruction of the Lower Devonian Cangwu Formation in southwestern China This figure shows the paleoecosystem with a coast setting.

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“…Such an affinity for Cangwuella is compatible with the morphological reconstruction for possible fossil shells of ancient arcellinid testate amoebae. 49 , 50 , 51 Our vase-shaped fossils show a close similarity of general shape to the ancestral Longithecina, although there is difference between them with respect to shell type. However, it should be borne in mind that 1) what the shell type (organic or agglutinated) of the most recent common ancestor of Arcellinida is remains an open question 51 ; 2) the reconstructed ancestor of Hyalosphenidae has an agglutinated shell, but there are indeed completely organic-shelled groups occurring in the extant hyalosphenids, e.g., Hyalosphenia papilio .…”

How good are global DNA‐based environmental surveys for detecting all protist diversity? Arcellinida as an example of biased representation

“…The salinity barrier does not seem to be an obstacle per se to the settlement of Arcellinida, as some species display a halotolerant metabolism (Useros et al, 2023). The probable absence of Arcellinida in fully marine ecosystems and the fact that these organisms are capable of adapting to high salinities suggests that biotic pressures (like predation or competition) prevent them from settling in the sea (Lahr, 2021; Useros et al, 2023).…”

“…The EukBank Arcellinida database also appeared to be strongly biased towards Phryganellina over suborders Organoconcha and Glutinoconcha. Indeed, the great majority of ASVs belonged to the suborder Phryganellina, a supposedly species-poor clade with only 46 described species distributed in four genera (Bobrov & Mazei, 2017, 2021Dumack et al, 2020). On the other hand, most of the over 630 species and 50 genera of the Glutinoconcha (Kosakyan et al, 2016) were not present in EukBank.…”

“…There were 687 nominal Arcellinida species in 2016 (Kosakyan et al, 2016), although many may need revision, and molecular studies have shown a high amount of cryptic diversity (Gonz alez-Miguéns, Soler-Zamora, et al, 2022;Kosakyan et al, 2012). Taxonomically, Arcellinida is divided into three suborders: Phryganellina, with only 46 described species (Bobrov & Mazei, 2017, 2021Dumack et al, 2020); Organoconcha, with about 15 species; and Glutinococha, the most conspicuous and well-studied suborder, comprising the great majority of the described Arcellinida species (>630). The latter suborder is divided into at least six infraorders .…”