Connecting the Dots: Does COI Variability in Paramecium caudatum (Ciliates, Protista) Support the Moderate Endemicity Model of Microeukaryote Distribution?

Abstract

Aim

Understanding the biodiversity and distribution patterns of microbial eukaryotes is fundamental to biosphere research. The biogeography of free-living protists remains contentious, with the ‘everything is everywhere’ and ‘moderate endemicity’ hypotheses representing competing paradigms. Here, we investigate whether and how global genetic variability within the cosmopolitan species Paramecium caudatum conforms to these models. We further examine whether genetic diversity within the COI gene can indicate the presence of cryptic species.

Location

Global study encompassing samples from nearly all major biogeographic realms, including the Palearctic, Nearctic, Neotropical, Indomalayan, and Australasian regions.

Time Period

Synthetic analysis combining historical data from public databases (GenBank) with newly collected data from strains isolated between 2015 and 2020.

Major Taxa Studied

The ciliate Paramecium caudatum.

Methods

We analysed the mitochondrial cytochrome c oxidase subunit I (COI) gene fragment from over 300 strains of P. caudatum, combining 231 newly sequenced samples with 103 sequences retrieved from the GenBank database. Phylogenetic relationships were reconstructed using maximum likelihood (ML), maximum parsimony (MP), neighbour-joining (NJ), and Bayesian inference (BI) methods. Haplotype networks were constructed using the median-joining method to assess genetic relationships and biogeographical patterns.

Results

Analysis revealed five distinct COI haplogroups (A, B, C, D and E) within a P. caudatum clade, each exhibiting distinct biogeographical signatures. Two haplogroups (A and B) displayed broad intercontinental distributions. In contrast, three others (C, D and E) showed restricted or endemic ranges, being confined to the Nearctic, northern Western Palearctic, and Indomalayan realms, respectively. The study revealed substantial intraspecific variability (Hd = 0.9252). Neutrality tests (Fu's F_s and Tajima's D) and congruence with previously published nuclear genomic data indicate that the major identified haplogroups are not random clusters but represent expanding evolutionary lineages.

Main Conclusions

Our findings demonstrate that while P. caudatum exhibits cosmopolitan distribution as a morphospecies, its intraspecific genetic structure displays pronounced heterogeneity at the global scale. The co-occurrence of haplogroups with contrasting distribution patterns, both widespread and endemic, provides compelling support for the moderate endemicity model in microbial eukaryote biogeography. These results underscore the existence of cryptic biodiversity and emphasise the need for high-resolution genetic analyses to gain a comprehensive understanding of microbial ecology and evolutionary processes.