Evolution of Traits Deduced from Genome Comparisons

Abstract

One of the major aims in evolutionary enomics is to leverage comparative genomic data sets to understand the evolution of adaptively important traits. These comparisons may occur at multiple scales, but can be roughly classed into those that focus on differences between closely related species and those that aim to explain broad patterns across diverse groups of organisms. Perhaps the most significant contributions of genome comparisons thus far have been in highlighting broad evolutionary trends, such as identifying gene sets or pathways that have been adaptively important in the evolution of specific lineages, including our own. In contrast, the establishment of concrete links between genetic variation and specific traits remains rare, despite a handful of exciting early successes. We anticipate that the addition of more genome sequences will rapidly advance the field. In particular, we look forward to increasing integration between comparative genomic analyses and ecological and phenotypic data sets.

Key concepts:

  • Comparisons between closely related species allow investigators to search for the genetic basis of recently evolved differences that distinguish those species.

  • Comparisons across organisms that share a distant common ancestor allow investigators to search for the genetic basis of major shared differences that define these groups of related organisms.

  • Genome comparisons often identify broad trends in trait evolution instead of specific genetic differences that influence a specific trait.

  • Identification of specific genes that influence a specific trait requires not only genome‐scale comparisons but also statistical filtering and experimental validation.

  • Identification of regions of the genome that evolved under positive selection or that are functionally important is a useful method for narrowing down genome‐wide differences to those that are most likely to have phenotypic effects.

Keywords: evolutionary genomics; sequence evolution; positive selection; phylogenetic comparisons; accelerated evolution

Figure 1.

Natural selection can be inferred from genome sequence comparisons. (a) Identification of unusually accelerated evolution in a functional region of the genome relative to a nearby region of the genome. In this example, the neutral rate of evolution is assessed by comparing differences among human, chimpanzee and rhesus macaque in the second intron of the gene. The upstream cis‐regulatory region of the same gene is evolving at about the same rate between chimpanzee and macaque, but has accumulated many more substitutions than expected from the intron data on the human lineage. This pattern suggests that the cis‐regulatory region in humans has been subject to repeated bouts of positive selection, and may make an important contribution to trait differences between humans and other primates. Bent arrow: start of transcription; rectangular boxes: transcribed exons (black: protein‐coding sequence; white; untranslated regions). (b) Identification of unusually accelerated evolution in an ultra‐conserved region of the genome. In this example, this stretch of DNA is highly conserved across mammals, suggesting an important functional role. However, the human lineage has accumulated multiple substitutions, suggesting occurrence of a functional change that affects only humans and that may have been subject to positive selection.

Figure 2.

Many sequence differences accrue between species (orange marks). To identify specific genetic changes underlying trait differences, genome sequence comparisons require further statistical or functional filtering. Two experimental designs are shown. (a) Genome‐wide functional data are collected, and differences between species are assessed based on these data (i.e. gene expression differences and transcription factor binding differences). These functional differences are then mapped to specific genes and genome sequence differences (purple shading). (b) Statistical filters (i.e. scans for selection) are first applied to genome sequence data to identify likely regions of interest (blue shading). Further experiments are conducted to determine if these regions are functionally differentiated between species. For example, reporter genes can be measured in cell culture to compare the levels of gene expression driven by a gene promoter region for each species.

Figure 3.

As more genome sequences become available, asking questions about broad patterns of evolution will become increasingly feasible. This figure depicts the relationships between 15 genera of monkeys and apes (note that the branch lengths are not to scale). Genera highlighted in blue are generally characterized as having monogamous social/mating systems; the remaining genera have other types of social system (designations from Smuts et al., ). Comparisons of genomic data across this tree may help elucidate the types of changes associated with monogamy in primates. Another set of questions arises from comparisons of closely related taxa in which one taxon is an ecological generalist and one taxon is relatively specialized. These pairs are highlighted in green: both humans and baboons are geographically widely distributed and do well in a large variety of ecological settings, whereas chimpanzees and geladas are ecologically more specialized and geographically more restricted.

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Further Reading

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Tung, Jenny, and Wray, Gregory A(Dec 2009) Evolution of Traits Deduced from Genome Comparisons. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0021746]