LTR Retroelements and Bird Adaptation to Arid Environments

Abstract

TEs are known to be among the main drivers in genome evolution, leading to the generation of evolutionary advantages that favor the success of organisms. The aim of this work was to investigate the TE landscape in bird genomes to look for a possible relationship between the amount of specific TE types and environmental changes that characterized the Oligocene era in Australia. Therefore, the mobilome of 29 bird species, belonging to a total of 11 orders, was analyzed. Our results confirmed that LINE retroelements are not predominant in all species of this evolutionary lineage and highlighted an LTR retroelement dominance in species with an Australian-related evolutionary history. The bird LTR retroelement expansion might have happened in response to the Earth's dramatic climate changes that occurred about 30 Mya, followed by a progressive aridification across most of Australian landmasses. Therefore, in birds, LTR retroelement burst might have represented an evolutionary advantage in the adaptation to arid/drought environments.

Keywords: Australian bird evolution; Aves; genome evolution; molecular adaptation; transposable elements; vertebrates.

Figure 1

Species considered in this study and their geographical distribution are shown. The landmasses are colored as follow: North and Central America in dark green; South America in light green; Africa in yellow; Antarctica in blue; Europe-Asia in orange; Australia in magenta; Indonesia and New Guinea in pink; New Zealand in purple. The colored square boxes indicate the geographical distribution of each species analyzed in this study.

Figure 2

The percentage of total transposable elements (TEs) masked in the genomes of the studied species. The histogram displays the percentage of the main TE types. * indicates species for which the analysis was performed on scaffold-level genome assembly.

Figure 3

Relative abundance of TE types in the mobilome of the bird species analyzed. * indicates species for which the analysis was performed on scaffold-level genome assembly.

Figure 4

Venn diagrams obtained by the variation partitioning analysis (VPA) using redundancy analysis (RDA). The partition of the variation of a response variable (X) between two sets of explanatory variables (X1 and X2) is shown. Each circle represents the portion of variation accounting for each explanatory variable or a combination of the explanatory matrices. The intersection between the two circles represents the amount of variation explained by both variables X1 and X2. The response variable (X) is the difference between the LTR retroelements relative abundances; the explanatory variable X1 represents species that have an ancestor that probably experienced an LTR expansion as consequence of climate changes that occurred in Australia and Antarctica during the Eocene-Oligocene transition; the explanatory variable X2 indicates the sequence divergence obtained by p-distance matrix using 16S rDNA sequences.

Figure 5

TE landscape plots obtained using Kimura distance-based copy divergence analyses of some species belonging to Neognathae (blue box) and Palaeognathae (red box). X axis: Kimura substitution level (CpG adjusted); Y axis: percent of genome. Panel (A) includes Passeriformes; panel (B) includes Psittaciformes; panel (C) includes Struthioniformes, Rheiformes, and Casuariformes.

Figure 6

Hypotheses suggested for A. aestiva and M. monachus evolutionary radiation. Panel (A): the ancestors of A. aestiva and M. monachus migrated from Australia to Antarctica (green arrow). The ancestor of A. aestiva migrated from Antarctica to South America before the dramatic cooling event occurred during the Eocene-Oligocene transition that led to the progressive aridification of Antarctica and Australian landmasses (blue arrow). The ancestor of M. monachus migrated from Antarctica to South America after this climate change event (orange arrow). Panel (B): the ancestors of A. aestiva and M. monachus migrated from Australia to Antarctica (green arrow) and then to South America after dramatic climate change events occurred about 30 Mya (orange arrow). Please see the discussion section for further details. For convenience, the current distribution of continents is shown.

Figure 7

On the left side biome-related distribution is reported for eight species considered in this study. The red box groups the Australian species; C. casuarius is distributed in New Guinea and in York Peninsula (far North Queensland, Australia); S. habroptila is an endemic species of New Zealand. In the geographical map the biomes present in these areas are colored according to the legend.