Speciation network in Laurasiatheria: retrophylogenomic signals

Abstract

Rapid species radiation due to adaptive changes or occupation of new ecospaces challenges our understanding of ancestral speciation and the relationships of modern species. At the molecular level, rapid radiation with successive speciations over short time periods-too short to fix polymorphic alleles-is described as incomplete lineage sorting. Incomplete lineage sorting leads to random fixation of genetic markers and hence, random signals of relationships in phylogenetic reconstructions. The situation is further complicated when you consider that the genome is a mosaic of ancestral and modern incompletely sorted sequence blocks that leads to reconstructed affiliations to one or the other relative, depending on the fixation of their shared ancestral polymorphic alleles. The laurasiatherian relationships among Chiroptera, Perissodactyla, Cetartiodactyla, and Carnivora present a prime example for such enigmatic affiliations. We performed whole-genome screenings for phylogenetically diagnostic retrotransposon insertions involving the representatives bat (Chiroptera), horse (Perissodactyla), cow (Cetartiodactyla), and dog (Carnivora), and extracted among 162,000 preselected cases 102 virtually homoplasy-free, phylogenetically informative retroelements to draw a complete picture of the highly complex evolutionary relations within Laurasiatheria. All possible evolutionary scenarios received considerable retrotransposon support, leaving us with a network of affiliations. However, the Cetartiodactyla-Carnivora relationship as well as the basal position of Chiroptera and an ancestral laurasiatherian hybridization process did exhibit some very clear, distinct signals. The significant accordance of retrotransposon presence/absence patterns and flanking nucleotide changes suggest an important influence of mosaic genome structures in the reconstruction of species histories.

Figure 1.

Retrotransposon-based network of the four investigated laurasiatherian orders. Numbers in balls represent the total number of retrotransposon insertions found for the respective order combination. Yellow balls represent markers merging two orders connected by the closest line. Gray balls represent markers merging the three orders arranged around the ball. The first framed number represents LINEs, the second LTRs, and the third (if present) the number of retropseudogenes.

Figure 2.

Phylogenetic network and phylogenetic tree reconstruction based on retrotransposon markers for the four investigated laurasiatherian orders. Neighbor-net (SplitsTree) analysis (left) and the most parsimonious tree reconstruction (Dollop in Phylip) (right) were conducted based on the presence/absence patterns of 102 retrotransposon insertions. Black numbers represent bootstrap values. The red number indicates the χ² significance value from the four-lineage insertion likelihood test (Supplemental Material S1) favoring the hybridization scenario merging horse with the bat and dog or dog/cow ancestor (red lines in the SplitsTree). An imaginary reconstruction of the Eomaia, an assumed ancestor of placentals, based on a description of Ji et al. (2002) is presented at the root of the “tree.”

Figure 3.

Ideogram representing the genomic locations of the 102 retrotransposon markers in the dog genome. The numbers to the left of the chromosomes represent the order pairs/triplets that are supported and serial number of the marker in that group. Six duplicated regions (but each with consensus presence/absence patterns) are indicated with lowercase letters (a–f). In addition, the colors of the numbers indicate the order pair/triplet affiliation to which the marker belongs, according to the legend at the bottom (Supplemental Table S1a): (Chi) Chiroptera, (Cet) Cetartiodactyla, (Car) Carnivora, (Per) Perissodactyla. The dog chromosome ideogram is based on the DAPI banded karyotype presented in Breen et al. (1999).