Abstract
A morphospecies is defined as a taxonomic species based wholly on morphology, but often morphospecies consist of clusters of cryptic species that can be identified genetically or molecularly. The nature of the evolutionary novelty that accompanies speciation in a morphospecies is an intriguing question. Morphospecies are particularly common among ciliates, a group of unicellular eukaryotes that separates 2 kinds of nuclei—the silenced germline nucleus (micronucleus [MIC]) and the actively expressed somatic nucleus (macronucleus [MAC])—within a common cytoplasm. Because of their very similar morphologies, members of the Tetrahymena genus are considered a morphospecies. We explored the hidden genomic evolution within this genus by performing a comprehensive comparative analysis of the somatic genomes of 10 species and the germline genomes of 2 species of Tetrahymena. These species show high genetic divergence; phylogenomic analysis suggests that the genus originated about 300 million years ago (Mya). Seven universal protein domains are preferentially included among the species-specific (i.e., the youngest) Tetrahymena genes. In particular, leucine-rich repeat (LRR) genes make the largest contribution to the high level of genome divergence of the 10 species. LRR genes can be sorted into 3 different age groups. Parallel evolutionary trajectories have independently occurred among LRR genes in the different Tetrahymena species. Thousands of young LRR genes contain tandem arrays of exactly 90-bp exons. The introns separating these exons show a unique, extreme phase 2 bias, suggesting a clonal origin and successive expansions of 90-bp–exon LRR genes. Identifying LRR gene age groups allowed us to document a Tetrahymena intron length cycle. The youngest 90-bp exon LRR genes in T. thermophila are concentrated in pericentromeric and subtelomeric regions of the 5 micronuclear chromosomes, suggesting that these regions act as genome innovation centers. Copies of a Tetrahymena Long interspersed element (LINE)-like retrotransposon are very frequently found physically adjacent to 90-bp exon/intron repeat units of the youngest LRR genes. We propose that Tetrahymena species have used a massive exon-shuffling mechanism, involving unequal crossing over possibly in concert with retrotransposition, to create the unique 90-bp exon array LRR genes.
Highlights
The species is one of the fundamental units of biology
Ten species of the Tetrahymena genus were selected for comparative analysis: T. thermophila, T. malaccensis, T. elliotti, T. pyriformis, T. vorax, T. borealis, T. canadensis, T. empidokyrea, T. shanghaiensis, and T. paravorax
In contrast to their similar morphological characteristics, a high level of genetic divergence was found among the 10 species, with genome sizes varying within a 1.4-fold range (84.9–114.8 Mb; Table 1), Guanine and Cytosine (GC) content varying from 20% to 29% (Table 1), and weak sequence similarity among the 10 genomes (S1 Fig)
Summary
The species is one of the fundamental units of biology. Defining a species has been a controversial issue for more than half a century, and there are more than 20 species concepts [1]. A large group of morphologically very similar Tetrahymena species were referred to as T. pyriformis [9]. Following the discovery of mating types in Tetrahymena, it was recognized that T. pyriformis is a morphospecies consisting of many reproductively isolated species and some asexual species [11, 12]. These species cannot be distinguished by ultrastructural morphology (such as cortical features revealed using protargol staining or electron microscopy), the number and size of micronuclear chromosomes, or tolerance to metals and high temperature [12]. Comparison of the ribosomal DNA (rDNA) sequences of these species suggested that they have high genetic divergence [9] and that the Tetrahymena genus is a few hundred million years old [13]
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