On the nature of species: insights from Paramecium and other ciliates

Abstract

The multiple species concepts currently in use by the scientific community (e.g. Morphological, Biological, Phylogenetic) are united in that they all aim to capture the process of divergence between populations. For example, the Biological Species Concept (BSC) defines a species as a natural group of organisms that is reproductively isolated from other such groups. Here we synthesize nearly a century of research on the ciliate genus Paramecium that highlights the shortcomings of our prevailing notions on the nature of species. In this lineage, there is discordance between morphology, mating behavior, and genetics, features assumed to be correlated, at least after sufficient time has passed, under all species concepts. Intriguingly, epigenetic phenomena are well documented in ciliates where they influence features such as germline/soma differentiation and mating type determination. Consequently, we hypothesize that divergence within ciliate populations is due to a dynamic interaction between genetic and epigenetic factors. The growing list of examples of epigenetic phenomena that potentially impact speciation (i.e. by influencing the dynamics of sex chromosomes, fate of hybrids, zygotic drive and genomic conflicts) suggests that interactions between genetics and epigenetics may also drive divergence in other eukaryotic lineages.

Insights into transgenerational epigenetics from studies of ciliates

“…Emmons and Lipton, 2003). In ciliates, mating types can be determined in at least three ways – synclonal, karyonidal and cytoplasmic – where the last two are epigenetically regulated (Hall and Katz, 2011; Phadke and Zufall, 2009). While synclonal inheritance follows Mendelian genetics, karyonidal and cytoplasmic inheritance are epigenetically regulated (Hall and Katz, 2011; Phadke and Zufall, 2009).…”

“…In ciliates, mating types can be determined in at least three ways – synclonal, karyonidal and cytoplasmic – where the last two are epigenetically regulated (Hall and Katz, 2011; Phadke and Zufall, 2009). While synclonal inheritance follows Mendelian genetics, karyonidal and cytoplasmic inheritance are epigenetically regulated (Hall and Katz, 2011; Phadke and Zufall, 2009). Karyonidal inheritance occurs when the mating type is determined either stochastically during macronuclear development or predictably by environmental stimuli such as temperature and light exposure (Figure 2C; Cervantes et al, 2013; Hall and Katz, 2011).…”

“…While synclonal inheritance follows Mendelian genetics, karyonidal and cytoplasmic inheritance are epigenetically regulated (Hall and Katz, 2011; Phadke and Zufall, 2009). Karyonidal inheritance occurs when the mating type is determined either stochastically during macronuclear development or predictably by environmental stimuli such as temperature and light exposure (Figure 2C; Cervantes et al, 2013; Hall and Katz, 2011). Cytoplasmic inheritance occurs when the mating type of the offspring reflects the parent’s phenotype, in a manner analogous to maternal inheritance in animals (Figure 2D; Hall and Katz, 2011; Phadke and Zufall, 2009; Sonneborn, 1977).…”

“…For examples, changes in gene copy number or locations of micronuclear-limited sequences in isolated populations may create barriers to genetic exchange, leading to rapid speciation events (Gao et al, 2015; Hall and Katz, 2011). Similarly, differential loss of duplicated macronuclear destined sequences, which can be corrected through gene unscrambling and alternative processing, may inhibit production of viable offspring between members of previously isolated populations (Gao et al, 2015).…”

“…Similarly, differential loss of duplicated macronuclear destined sequences, which can be corrected through gene unscrambling and alternative processing, may inhibit production of viable offspring between members of previously isolated populations (Gao et al, 2015). This rapid speciation as the result of epigenetic processes may contribute to the complex patterns of morphological and molecular evolution such as cryptic species, which are common in ciliates (Foissner et al, 2008; Hall and Katz, 2011; Lahr et al, 2014; Przybos and Tarcz, 2016; Sonneborn, 1975). …”