Literature DB >> 26755583

Testing the kinship theory of intragenomic conflict in honey bees (Apis mellifera).

David A Galbraith1, Sarah D Kocher2, Tom Glenn3, Istvan Albert4, Greg J Hunt5, Joan E Strassmann6, David C Queller6, Christina M Grozinger1.   

Abstract

Sexual reproduction brings genes from two parents (matrigenes and patrigenes) together into one individual. These genes, despite being unrelated, should show nearly perfect cooperation because each gains equally through the production of offspring. However, an individual's matrigenes and patrigenes can have different probabilities of being present in other relatives, so kin selection could act on them differently. Such intragenomic conflict could be implemented by partial or complete silencing (imprinting) of an allele by one of the parents. Evidence supporting this theory is seen in offspring-mother interactions, with patrigenes favoring acquisition of more of the mother's resources if some of the costs fall on half-siblings who do not share the patrigene. The kinship theory of intragenomic conflict is little tested in other contexts, but it predicts that matrigene-patrigene conflict may be rife in social insects. We tested the hypothesis that honey bee worker reproduction is promoted more by patrigenes than matrigenes by comparing across nine reciprocal crosses of two distinct genetic stocks. As predicted, hybrid workers show reproductive trait characteristics of their paternal stock, (indicating enhanced activity of the patrigenes on these traits), greater patrigenic than matrigenic expression, and significantly increased patrigenic-biased expression in reproductive workers. These results support both the general prediction that matrigene-patrigene conflict occurs in social insects and the specific prediction that honey bee worker reproduction is driven more by patrigenes. The success of these predictions suggests that intragenomic conflict may occur in many contexts where matrigenes and patrigenes have different relatednesses to affected kin.

Entities:  

Keywords:  evolutionary biology; intragenomic conflict; kinship theory; social insects; sociogenomics

Mesh:

Year:  2016        PMID: 26755583      PMCID: PMC4743802          DOI: 10.1073/pnas.1516636113

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  44 in total

1.  Using pyrosequencing to measure allele-specific mRNA abundance and infer the effects of cis- and trans-regulatory differences.

Authors:  Patricia J Wittkopp
Journal:  Methods Mol Biol       Date:  2011

2.  Reproductive protein protects functionally sterile honey bee workers from oxidative stress.

Authors:  Siri-Christine Seehuus; Kari Norberg; Ulrike Gimsa; Trygve Krekling; Gro V Amdam
Journal:  Proc Natl Acad Sci U S A       Date:  2006-01-17       Impact factor: 11.205

Review 3.  Using next-generation RNA sequencing to identify imprinted genes.

Authors:  X Wang; A G Clark
Journal:  Heredity (Edinb)       Date:  2014-03-12       Impact factor: 3.821

Review 4.  Molecular biology of mosquito vitellogenesis: from basic studies to genetic engineering of antipathogen immunity.

Authors:  Alexander S Raikhel; Vladimir A Kokoza; Jinsong Zhu; David Martin; Sheng-Fu Wang; Chao Li; Guoqiang Sun; Abdoulaziz Ahmed; Neal Dittmer; Geoff Attardo
Journal:  Insect Biochem Mol Biol       Date:  2002-10       Impact factor: 4.714

5.  The genetic basis of transgressive ovary size in honeybee workers.

Authors:  Timothy A Linksvayer; Olav Rueppell; Adam Siegel; Osman Kaftanoglu; Robert E Page; Gro V Amdam
Journal:  Genetics       Date:  2009-07-20       Impact factor: 4.562

6.  Parallel epigenomic and transcriptomic responses to viral infection in honey bees (Apis mellifera).

Authors:  David A Galbraith; Xingyu Yang; Elina Lastro Niño; Soojin Yi; Christina Grozinger
Journal:  PLoS Pathog       Date:  2015-03-26       Impact factor: 6.823

7.  Theory of genomic imprinting conflict in social insects.

Authors:  David C Queller
Journal:  BMC Evol Biol       Date:  2003-07-18       Impact factor: 3.260

8.  Transcriptome-wide identification of novel imprinted genes in neonatal mouse brain.

Authors:  Xu Wang; Qi Sun; Sean D McGrath; Elaine R Mardis; Paul D Soloway; Andrew G Clark
Journal:  PLoS One       Date:  2008-12-04       Impact factor: 3.240

9.  Finding the missing honey bee genes: lessons learned from a genome upgrade.

Authors:  Christine G Elsik; Kim C Worley; Anna K Bennett; Martin Beye; Francisco Camara; Christopher P Childers; Dirk C de Graaf; Griet Debyser; Jixin Deng; Bart Devreese; Eran Elhaik; Jay D Evans; Leonard J Foster; Dan Graur; Roderic Guigo; Katharina Jasmin Hoff; Michael E Holder; Matthew E Hudson; Greg J Hunt; Huaiyang Jiang; Vandita Joshi; Radhika S Khetani; Peter Kosarev; Christie L Kovar; Jian Ma; Ryszard Maleszka; Robin F A Moritz; Monica C Munoz-Torres; Terence D Murphy; Donna M Muzny; Irene F Newsham; Justin T Reese; Hugh M Robertson; Gene E Robinson; Olav Rueppell; Victor Solovyev; Mario Stanke; Eckart Stolle; Jennifer M Tsuruda; Matthias Van Vaerenbergh; Robert M Waterhouse; Daniel B Weaver; Charles W Whitfield; Yuanqing Wu; Evgeny M Zdobnov; Lan Zhang; Dianhui Zhu; Richard A Gibbs
Journal:  BMC Genomics       Date:  2014-01-30       Impact factor: 3.969

10.  Genome-wide and caste-specific DNA methylomes of the ants Camponotus floridanus and Harpegnathos saltator.

Authors:  Roberto Bonasio; Qiye Li; Jinmin Lian; Navdeep S Mutti; Lijun Jin; Hongmei Zhao; Pei Zhang; Ping Wen; Hui Xiang; Yun Ding; Zonghui Jin; Steven S Shen; Zongji Wang; Wen Wang; Jun Wang; Shelley L Berger; Jürgen Liebig; Guojie Zhang; Danny Reinberg
Journal:  Curr Biol       Date:  2012-08-09       Impact factor: 10.834

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  18 in total

1.  Sociality emerges from solitary behaviours and reproductive plasticity in the orchid bee Euglossa dilemma.

Authors:  Nicholas W Saleh; Santiago R Ramírez
Journal:  Proc Biol Sci       Date:  2019-07-10       Impact factor: 5.349

2.  Caste-biased gene expression in a facultatively eusocial bee suggests a role for genetic accommodation in the evolution of eusociality.

Authors:  Beryl M Jones; Callum J Kingwell; William T Wcislo; Gene E Robinson
Journal:  Proc Biol Sci       Date:  2017-01-11       Impact factor: 5.349

Review 3.  Parent-of-origin effects, allele-specific expression, genomic imprinting and paternal manipulation in social insects.

Authors:  Benjamin P Oldroyd; Boris Yagound
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2021-04-19       Impact factor: 6.671

4.  How does epigenetics influence the course of evolution?

Authors:  Alyson Ashe; Vincent Colot; Benjamin P Oldroyd
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2021-04-19       Impact factor: 6.671

5.  Parent-of-origin effects on genome-wide DNA methylation in the Cape honey bee (Apis mellifera capensis) may be confounded by allele-specific methylation.

Authors:  Emily J Remnant; Alyson Ashe; Paul E Young; Gabriele Buchmann; Madeleine Beekman; Michael H Allsopp; Catherine M Suter; Robert A Drewell; Benjamin P Oldroyd
Journal:  BMC Genomics       Date:  2016-03-12       Impact factor: 3.969

6.  Genome methylation patterns across castes and generations in a parasitoid wasp.

Authors:  Roei Shaham; Rachel Ben-Shlomo; Uzi Motro; Tamar Keasar
Journal:  Ecol Evol       Date:  2016-09-30       Impact factor: 2.912

7.  Sexual selection modulates genetic conflicts and patterns of genomic imprinting.

Authors:  Gonçalo S Faria; Susana A M Varela; Andy Gardner
Journal:  Evolution       Date:  2017-01-16       Impact factor: 3.694

8.  Intragroup and intragenomic conflict over chemical defense against predators.

Authors:  Rebekah Best; Graeme D Ruxton; Andy Gardner
Journal:  Ecol Evol       Date:  2018-02-19       Impact factor: 2.912

9.  Allele-Specific Transcriptome and Methylome Analysis Reveals Stable Inheritance and Cis-Regulation of DNA Methylation in Nasonia.

Authors:  Xu Wang; John H Werren; Andrew G Clark
Journal:  PLoS Biol       Date:  2016-07-05       Impact factor: 8.029

Review 10.  Building a new research framework for social evolution: intralocus caste antagonism.

Authors:  Tanya M Pennell; Luke Holman; Edward H Morrow; Jeremy Field
Journal:  Biol Rev Camb Philos Soc       Date:  2018-01-16
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