Vocal learning-associated convergent evolution in mammalian proteins and regulatory elements.

Vocal production learning ("vocal learning") is a convergently evolved trait in vertebrates. To identify brain genomic elements associated with mammalian vocal learning, we integrated genomic, anatomical, and neurophysiological data from the Egyptian fruit bat (Rousettus aegyptiacus) with analyses of the genomes of 215 placental mammals. First, we identified a set of proteins evolving more slowly in vocal learners. Then, we discovered a vocal motor cortical region in the Egyptian fruit bat, an emergent vocal learner, and leveraged that knowledge to identify active cis-regulatory elements in the motor cortex of vocal learners. Machine learning methods applied to motor cortex open chromatin revealed 50 enhancers robustly associated with vocal learning whose activity tended to be lower in vocal learners. Our research implicates convergent losses of motor cortex regulatory elements in mammalian vocal learning evolution.

Insights into mammalian TE diversity through the curation of 248 genome assemblies.

We examined transposable element (TE) content of 248 placental mammal genome assemblies, the largest de novo TE curation effort in eukaryotes to date. We found that although mammals resemble one another in total TE content and diversity, they show substantial differences with regard to recent TE accumulation. This includes multiple recent expansion and quiescence events across the mammalian tree. Young TEs, particularly long interspersed elements, drive increases in genome size, whereas DNA transposons are associated with smaller genomes. Mammals tend to accumulate only a few types of TEs at any given time, with one TE type dominating. We also found association between dietary habit and the presence of DNA transposon invasions. These detailed annotations will serve as a benchmark for future comparative TE analyses among placental mammals.

Chiropterans Are a Hotspot for Horizontal Transfer of DNA Transposons in Mammalia.

Horizontal transfer of transposable elements (TEs) is an important mechanism contributing to genetic diversity and innovation. Bats (order Chiroptera) have repeatedly been shown to experience horizontal transfer of TEs at what appears to be a high rate compared with other mammals. We investigated the occurrence of horizontally transferred (HT) DNA transposons involving bats. We found over 200 putative HT elements within bats; 16 transposons were shared across distantly related mammalian clades, and 2 other elements were shared with a fish and two lizard species. Our results indicate that bats are a hotspot for horizontal transfer of DNA transposons. These events broadly coincide with the diversification of several bat clades, supporting the hypothesis that DNA transposon invasions have contributed to genetic diversification of bats.

Comparison of genetic variation between rare and common congeners of Dipodomys with estimates of contemporary and historical effective population size.

Species with low effective population sizes are at greater risk of extinction because of reduced genetic diversity. Such species are more vulnerable to chance events that decrease population sizes (e.g. demographic stochasticity). Dipodomys elator, (Texas kangaroo rat) is a kangaroo rat that is classified as threatened in Texas and field surveys from the past 50 years indicate that the distribution of this species has decreased. This suggests geographic range reductions that could have caused population fluctuations, potentially impacting effective population size. Conversely, the more common and widespread D. ordii (Ord's kangaroo rat) is thought to exhibit relative geographic and demographic stability. We assessed the genetic variation of D. elator and D. ordii samples using 3RAD, a modified restriction site associated sequencing approach. We hypothesized that D. elator would show lower levels of nucleotide diversity, observed heterozygosity, and effective population size when compared to D. ordii. We were also interested in identifying population structure within contemporary samples of D. elator and detecting genetic variation between temporal samples to understand demographic dynamics. We analyzed up to 61,000 single nucleotide polymorphisms. We found that genetic variability and effective population size in contemporary D. elator populations is lower than that of D. ordii. There is slight, if any, population structure within contemporary D. elator samples, and we found low genetic differentiation between spatial or temporal historical samples. This indicates little change in nuclear genetic diversity over 30 years. Results suggest that genetic diversity of D. elator has remained stable despite reduced population size and/or abundance, which may indicate a metapopulation-like system, whose fluctuations might counteract species extinction.

Simultaneous TE Analysis of 19 Heliconiine Butterflies Yields Novel Insights into Rapid TE-Based Genome Diversification and Multiple SINE Births and Deaths.

Transposable elements (TEs) play major roles in the evolution of genome structure and function. However, because of their repetitive nature, they are difficult to annotate and discovering the specific roles they may play in a lineage can be a daunting task. Heliconiine butterflies are models for the study of multiple evolutionary processes including phenotype evolution and hybridization. We attempted to determine how TEs may play a role in the diversification of genomes within this clade by performing a detailed examination of TE content and accumulation in 19 species whose genomes were recently sequenced. We found that TE content has diverged substantially and rapidly in the time since several subclades shared a common ancestor with each lineage harboring a unique TE repertoire. Several novel SINE lineages have been established that are restricted to a subset of species. Furthermore, the previously described SINE, Metulj, appears to have gone extinct in two subclades while expanding to significant numbers in others. This diversity in TE content and activity has the potential to impact how heliconiine butterflies continue to evolve and diverge.