Genomic signatures of evolutionary transitions from solitary to group living

Karen M. Kapheim; Hailin Pan; Cai Li; Steven L. Salzberg; Daniela Puiu; Tanja Magoc; Hugh M. Robertson; Matthew E. Hudson; Aarti Venkat; Brielle J. Fischman; Alvaro Hernandez; Mark Yandell; Daniel Ence; Carson Holt; George D Yocum; William P. Kemp; Jordi Bosch; Robert M Waterhouse; Evgeny M Zdobnov; Eckart Stolle; F. Bernhard Kraus; Sophie Helbing; Robin F. A. Moritz; Karl M. Glastad; Brendan G. Hunt; Michael A. D. Goodisman; Frank Hauser; Cornelis Grimmelikhuijzen; Daniel Guariz Pinheiro; Francis Morais Franco Nunes; Michelle Prioli Miranda Soares; Érica Donato Tanaka; Zilá Luz Paulino Simões; Klaus Hartfelder; Jay D. Evans; Seth M. Barribeau; Reed M. Johnson; Jonathan H. Massey; Bruce R. Southey; Martin Hasselmann; Daniel Hamacher; Matthias Biewer; Clement F. Kent; Amro Zayed; Charles Blatti; Saurabh Sinha; J. Spencer Johnston; Shawn J. Hanrahan; Sarah D. Kocher; Jun Wang; Gene E. Robinson; Guojie Zhang

doi:10.1126/science.aaa4788

Genomic signatures of evolutionary transitions from solitary to group living

Karen M. Kapheim, Hailin Pan, Cai Li, Steven L. Salzberg, Daniela Puiu, Tanja Magoc, Hugh M. Robertson, Matthew E. Hudson, Aarti Venkat, Brielle J. Fischman, Alvaro Hernandez, Mark Yandell, Daniel Ence, Carson Holt, George D Yocum, William P. Kemp, Jordi Bosch, Robert M Waterhouse, Evgeny M Zdobnov, Eckart StolleF. Bernhard Kraus, Sophie Helbing, Robin F. A. Moritz, Karl M. Glastad, Brendan G. Hunt, Michael A. D. Goodisman, Frank Hauser, Cornelis Grimmelikhuijzen, Daniel Guariz Pinheiro, Francis Morais Franco Nunes, Michelle Prioli Miranda Soares, Érica Donato Tanaka, Zilá Luz Paulino Simões, Klaus Hartfelder, Jay D. Evans, Seth M. Barribeau, Reed M. Johnson, Jonathan H. Massey, Bruce R. Southey, Martin Hasselmann, Daniel Hamacher, Matthias Biewer, Clement F. Kent, Amro Zayed, Charles Blatti, Saurabh Sinha, J. Spencer Johnston, Shawn J. Hanrahan, Sarah D. Kocher, Jun Wang, Gene E. Robinson, Guojie Zhang

191 Citations (Scopus)

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.

Original language	English
Journal	Science (New York, N.Y.)
Volume	348
Issue number	6239
Pages (from-to)	1139-1143
Number of pages	5
ISSN	0036-8075
DOIs	https://doi.org/10.1126/science.aaa4788
Publication status	Published - 5 Jun 2015

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Kapheim, K. M., Pan, H., Li, C., Salzberg, S. L., Puiu, D., Magoc, T., Robertson, H. M., Hudson, M. E., Venkat, A., Fischman, B. J., Hernandez, A., Yandell, M., Ence, D., Holt, C., Yocum, G. D., Kemp, W. P., Bosch, J., Waterhouse, R. M., Zdobnov, E. M., ... Zhang, G. (2015). Genomic signatures of evolutionary transitions from solitary to group living. Science (New York, N.Y.), 348(6239), 1139-1143. https://doi.org/10.1126/science.aaa4788

Kapheim, KM, Pan, H, Li, C, Salzberg, SL, Puiu, D, Magoc, T, Robertson, HM, Hudson, ME, Venkat, A, Fischman, BJ, Hernandez, A, Yandell, M, Ence, D, Holt, C, Yocum, GD, Kemp, WP, Bosch, J, Waterhouse, RM, Zdobnov, EM, Stolle, E, Kraus, FB, Helbing, S, Moritz, RFA, Glastad, KM, Hunt, BG, Goodisman, MAD, Hauser, F , Grimmelikhuijzen, C, Pinheiro, DG, Nunes, FMF, Soares, MPM, Tanaka, ÉD, Simões, ZLP, Hartfelder, K, Evans, JD, Barribeau, SM, Johnson, RM, Massey, JH, Southey, BR, Hasselmann, M, Hamacher, D, Biewer, M, Kent, CF, Zayed, A, Blatti, C, Sinha, S, Johnston, JS, Hanrahan, SJ, Kocher, SD, Wang, J, Robinson, GE & Zhang, G 2015, 'Genomic signatures of evolutionary transitions from solitary to group living', Science (New York, N.Y.), vol. 348, no. 6239, pp. 1139-1143. https://doi.org/10.1126/science.aaa4788

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title = "Genomic signatures of evolutionary transitions from solitary to group living",

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.",

author = "Kapheim, {Karen M.} and Hailin Pan and Cai Li and Salzberg, {Steven L.} and Daniela Puiu and Tanja Magoc and Robertson, {Hugh M.} and Hudson, {Matthew E.} and Aarti Venkat and Fischman, {Brielle J.} and Alvaro Hernandez and Mark Yandell and Daniel Ence and Carson Holt and Yocum, {George D} and Kemp, {William P.} and Jordi Bosch and Waterhouse, {Robert M} and Zdobnov, {Evgeny M} and Eckart Stolle and Kraus, {F. Bernhard} and Sophie Helbing and Moritz, {Robin F. A.} and Glastad, {Karl M.} and Hunt, {Brendan G.} and Goodisman, {Michael A. D.} and Frank Hauser and Cornelis Grimmelikhuijzen and Pinheiro, {Daniel Guariz} and Nunes, {Francis Morais Franco} and Soares, {Michelle Prioli Miranda} and Tanaka, {{\'E}rica Donato} and Sim{\~o}es, {Zil{\'a} Luz Paulino} and Klaus Hartfelder and Evans, {Jay D.} and Barribeau, {Seth M.} and Johnson, {Reed M.} and Massey, {Jonathan H.} and Southey, {Bruce R.} and Martin Hasselmann and Daniel Hamacher and Matthias Biewer and Kent, {Clement F.} and Amro Zayed and Charles Blatti and Saurabh Sinha and Johnston, {J. Spencer} and Hanrahan, {Shawn J.} and Kocher, {Sarah D.} and Jun Wang and Robinson, {Gene E.} and Guojie Zhang",

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AU - Kapheim, Karen M.

AU - Pan, Hailin

AU - Li, Cai

AU - Salzberg, Steven L.

AU - Puiu, Daniela

AU - Magoc, Tanja

AU - Robertson, Hugh M.

AU - Hudson, Matthew E.

AU - Venkat, Aarti

AU - Fischman, Brielle J.

AU - Hernandez, Alvaro

AU - Yandell, Mark

AU - Ence, Daniel

AU - Holt, Carson

AU - Yocum, George D

AU - Kemp, William P.

AU - Bosch, Jordi

AU - Waterhouse, Robert M

AU - Zdobnov, Evgeny M

AU - Stolle, Eckart

AU - Kraus, F. Bernhard

AU - Helbing, Sophie

AU - Moritz, Robin F. A.

AU - Glastad, Karl M.

AU - Hunt, Brendan G.

AU - Goodisman, Michael A. D.

AU - Hauser, Frank

AU - Grimmelikhuijzen, Cornelis

AU - Pinheiro, Daniel Guariz

AU - Nunes, Francis Morais Franco

AU - Soares, Michelle Prioli Miranda

AU - Tanaka, Érica Donato

AU - Simões, Zilá Luz Paulino

AU - Hartfelder, Klaus

AU - Evans, Jay D.

AU - Barribeau, Seth M.

AU - Johnson, Reed M.

AU - Massey, Jonathan H.

AU - Southey, Bruce R.

AU - Hasselmann, Martin

AU - Hamacher, Daniel

AU - Biewer, Matthias

AU - Kent, Clement F.

AU - Zayed, Amro

AU - Blatti, Charles

AU - Sinha, Saurabh

AU - Johnston, J. Spencer

AU - Hanrahan, Shawn J.

AU - Kocher, Sarah D.

AU - Wang, Jun

AU - Robinson, Gene E.

AU - Zhang, Guojie

PY - 2015/6/5

Y1 - 2015/6/5

N2 - 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.

AB - 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.

U2 - 10.1126/science.aaa4788

DO - 10.1126/science.aaa4788

M3 - Journal article

C2 - 25977371

SN - 0036-8075

VL - 348

SP - 1139

EP - 1143

JO - Science

JF - Science

IS - 6239

ER -

Genomic signatures of evolutionary transitions from solitary to group living

Abstract

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