Mosaic retroposon insertion patterns in placental mammals

Abstract

One and a half centuries after Charles Darwin and Alfred Russel Wallace outlined our current understanding of evolution, a new scientific era is dawning that enables direct observations of genetic variation. However, pure sequence-based molecular attempts to resolve the basal origin of placental mammals have so far resulted only in apparently conflicting hypotheses. By contrast, in the mammalian genomes where they were highly active, the insertion of retroelements and their comparative insertion patterns constitute a neutral, virtually homoplasy-free archive of evolutionary histories. The ''presence'' of a retroelement at an orthologous genomic position in two species indicates their common ancestry in contrast to its ''absence'' in more distant species. To resolve the placental origin controversy we extracted ;2 million potentially phylogenetically informative, retroposon-containing loci from representatives of the major placental mammalian lineages and found highly significant evidence challenging all current single hypotheses of their basal origin. The Exafroplacentalia hypothesis (Afrotheria as the sister group to all remaining placentals) is significantly supported by five retroposon insertions, the Epitheria hypothesis (Xenarthra as the sister group to all remaining placentals) by nine insertion patterns, and the Atlantogenata hypothesis (a monophyletic clade comprising Xenarthra and Afrotheria as the sister group to Boreotheria comprising all remaining placentals) by eight insertion patterns. These findings provide significant support for a ''soft'' polytomy of the major mammalian clades. Ancestral successive hybridization events and/ or incomplete lineage sorting associated with short speciation intervals are viable explanations for the mosaic retroposon insertion patterns of recent placental mammals and for the futile search for a clear root dichotomy.

Ultraconserved elements are novel phylogenomic markers that resolve placental mammal phylogeny when combined with species-tree analysis

“…Even more spectacular is the explosive radiation of orders within the Laurasiatheria (e.g., dogs, bats, horses, cows, dolphins), with several basal splits occurring within 1 to 3 million years of one another (Springer et al 2003). As predicted by coalescent theory (Degnan and Salter 2005), these are the same divergences where individual gene trees give conflicting answers about evolutionary relationships (Nishihara et al 2006(Nishihara et al , 2009Murphy et al 2007;Churakov et al 2009), underscoring the need for an approach that incorporates a model of the process at the root of this discord-coalescent stochasticity. This is especially relevant given the recent discovery of a phylogenetic anomaly zone where rapid speciation results in the most common gene tree being in conflict with the true species history (Degnan and Rosenberg 2006), a situation that will mislead phylogenetic inference unless coalescent stochasticity is taken into account (Kubatko and Degnan 2007).…”

The new framework for understanding placental mammal evolution

“…Although some ambiguity and points of contention remain, (13,14) the trend of genomic-scale phylogenetics for living mammals continues. (15,16) Extended taxon sampling applied to mitochondrial genomes, (17,18) together with analyses of chromosomal data, (19) are largely consistent with the nuclear-genomic phylogenies that sample across placental mammal orders, supporting the basic topology first made explicit at the turn of this century. (20)(21)(22)(23) While this consensus has yielded some ambiguous is now resolved into a well-supported, high-level phylogeny ( Fig.…”

“…(15) Many recent studies support Afrotheria and Xenarthra as sister taxa in Atlantogenata, (6,7,9,15,17,20,29) but confidence in this result remains elusive. Further evaluation of the statistical support of the Atlantogenata hypothesis (31) and scrutiny of homoplasy in an allegedly ''homoplasy-free'' class of retroposon data (16,30) suggest that the placental root is still not adequately resolved. Fortunately, there are only two seriously considered alternatives for the placental root: ''Epitheria'', first suggested by McKenna, (26,31) and ''Exafroplacentalia'', (8,22,32,33) in which Xenarthra or Afrotheria (respectively) comprise the basal-most placental clade.…”

Rates and patterns of great ape retrotransposition

“…Our results more than triple the number of known polymorphic MEIs in great apes, including the discovery of ancestry-informative markers and MEIs corresponding to regions of incomplete lineage sorting (ILS). Such ILS segments define regions where the gene genealogy differs from that of the species phylogeny due to rapid speciation or hybridization and are relatively rare, especially as defined by the MEI (19,30,31). The availability of single-nucleotide polymorphism (SNP) data (32) from the same individual genomes allows us to more accurately estimate rate changes in Alu and L1 retrotransposition in contrast to single-nucleotide accumulation and to compare the utility of these markers in reconstructing the evolutionary relationships of our species.…”