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Comparative Study
. 2015 Jun 5;348(6239):1139-43.
doi: 10.1126/science.aaa4788. Epub 2015 May 14.

Social evolution. Genomic signatures of evolutionary transitions from solitary to group living

Affiliations
Comparative Study

Social evolution. Genomic signatures of evolutionary transitions from solitary to group living

Karen M Kapheim et al. Science. .

Abstract

The evolution of eusociality is one of the major transitions in evolution, but the underlying genomic changes are unknown. We compared the genomes of 10 bee species that vary in social complexity, representing multiple independent transitions in social evolution, and report three major findings. First, many important genes show evidence of neutral evolution as a consequence of relaxed selection with increasing social complexity. Second, there is no single road map to eusociality; independent evolutionary transitions in sociality have independent genetic underpinnings. Third, though clearly independent in detail, these transitions do have similar general features, including an increase in constrained protein evolution accompanied by increases in the potential for gene regulation and decreases in diversity and abundance of transposable elements. Eusociality may arise through different mechanisms each time, but would likely always involve an increase in the complexity of gene networks.

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Figures

Fig. 1
Fig. 1. Phylogeny and divergence times (28) of bees selected for genome analysis
We analyzed two independent origins of simple eusociality from a solitary ancestor, one each in Apidae (white circle 1) and Halictidae (white circle 2), and two independent elaborations of complex eusociality in honeybees (gray circle 1) and stingless bees (gray circle 2). Most bees mate once, but honeybees mate with multiple males. All bees eat pollen and nectar from flowering plants. Species names are colored according to degree of social complexity: blue: ancestrally solitary; green: facultative simple eusociality; orange: obligate simple eusociality; red: obligate complex eusociality. The social biology of E. mexicana is unknown, but is representative of the facultative simple eusocial life history (29). Numbers in each box are approximate colony size on a log scale. MRCA, most recent common ancestor; mya, millions of years ago.
Fig. 2
Fig. 2. Genomic signatures of evolutionary transitions from solitary to group life
(A) Increasing social complexity is associated with increasing presence of cis-regulatory TFBSs in promoter regions. Each bar represents a TFBS for which presence correlates significantly with social complexity (blue: positive; red: negative). (B) Relationship between predicted numberof methylated genes and social complexity before and after (inset) phylogenetic correction (see text for statistics). (C) TFBS motifs showing a relationship between social complexity and evolutionary rate of coding and noncoding sequences in different lineages. Bar length indicates the number of significant correlations (blue: positive; red: negative) between each motif score and social complexity (from Table 1) among genes evolving faster (solid) or slower (hatched) in lineages with different levels of social complexity [from (D)]. Background shading follows circle shading in Fig. 1. (D) Number of genes for which evolutionary rate is faster or slower in lineages with higher compared to lower social complexity. Pie charts represent the proportion of genes evolving slower (light green) or faster (dark orange) with increased social complexity. Venn diagram shading follows circle shading in Fig. 1. (E) Complex eusocial species have a reduced proportion of repetitive DNA compared to other bees (see text for statistics). LTR, long terminal repeat; LINE, long interspersed element; SINE, short interspersed element; DNA, DNA transposon; LARD, large retrotransposon derivative; TRIM, terminal repeat retrotransposon in miniature; MITE, miniature inverted-repeat transposable element; TES, transposable elements.

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