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Disentangling prenatal and postnatal maternal genetic effects reveals persistent prenatal effects on offspring growth in mice
Mothers are often the most important determinant of traits expressed by their offspring. These "maternal effects" (MEs) are especially crucial in early development, but can also persist into adulthood. They have been shown to play a role in a diversity of evolutionary and ecological proces...
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Published in: | Genetics (Austin) 2011-11, Vol.189 (3), p.1069-1082 |
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description | Mothers are often the most important determinant of traits expressed by their offspring. These "maternal effects" (MEs) are especially crucial in early development, but can also persist into adulthood. They have been shown to play a role in a diversity of evolutionary and ecological processes, especially when genetically based. Although the importance of MEs is becoming widely appreciated, we know little about their underlying genetic basis. We address the dearth of genetic data by providing a simple approach, using combined genotype information from parents and offspring, to identify "maternal genetic effects" (MGEs) contributing to natural variation in complex traits. Combined with experimental cross-fostering, our approach also allows for the separation of pre- and postnatal MGEs, providing rare insights into prenatal effects. Applying this approach to an experimental mouse population, we identified 13 ME loci affecting body weight, most of which (12/13) exhibited prenatal effects, and nearly half (6/13) exhibiting postnatal effects. MGEs contributed more to variation in body weight than the direct effects of the offsprings' own genotypes until mice reached adulthood, but continued to represent a major component of variation through adulthood. Prenatal effects always contributed more variation than postnatal effects, especially for those effects that persisted into adulthood. These results suggest that MGEs may be an important component of genetic architecture that is generally overlooked in studies focused on direct mapping from genotype to phenotype. Our approach can be used in both experimental and natural populations, providing a widely practicable means of expanding our understanding of MGEs. |
doi_str_mv | 10.1534/genetics.111.130591 |
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These "maternal effects" (MEs) are especially crucial in early development, but can also persist into adulthood. They have been shown to play a role in a diversity of evolutionary and ecological processes, especially when genetically based. Although the importance of MEs is becoming widely appreciated, we know little about their underlying genetic basis. We address the dearth of genetic data by providing a simple approach, using combined genotype information from parents and offspring, to identify "maternal genetic effects" (MGEs) contributing to natural variation in complex traits. Combined with experimental cross-fostering, our approach also allows for the separation of pre- and postnatal MGEs, providing rare insights into prenatal effects. Applying this approach to an experimental mouse population, we identified 13 ME loci affecting body weight, most of which (12/13) exhibited prenatal effects, and nearly half (6/13) exhibiting postnatal effects. MGEs contributed more to variation in body weight than the direct effects of the offsprings' own genotypes until mice reached adulthood, but continued to represent a major component of variation through adulthood. Prenatal effects always contributed more variation than postnatal effects, especially for those effects that persisted into adulthood. These results suggest that MGEs may be an important component of genetic architecture that is generally overlooked in studies focused on direct mapping from genotype to phenotype. 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These "maternal effects" (MEs) are especially crucial in early development, but can also persist into adulthood. They have been shown to play a role in a diversity of evolutionary and ecological processes, especially when genetically based. Although the importance of MEs is becoming widely appreciated, we know little about their underlying genetic basis. We address the dearth of genetic data by providing a simple approach, using combined genotype information from parents and offspring, to identify "maternal genetic effects" (MGEs) contributing to natural variation in complex traits. Combined with experimental cross-fostering, our approach also allows for the separation of pre- and postnatal MGEs, providing rare insights into prenatal effects. Applying this approach to an experimental mouse population, we identified 13 ME loci affecting body weight, most of which (12/13) exhibited prenatal effects, and nearly half (6/13) exhibiting postnatal effects. MGEs contributed more to variation in body weight than the direct effects of the offsprings' own genotypes until mice reached adulthood, but continued to represent a major component of variation through adulthood. Prenatal effects always contributed more variation than postnatal effects, especially for those effects that persisted into adulthood. These results suggest that MGEs may be an important component of genetic architecture that is generally overlooked in studies focused on direct mapping from genotype to phenotype. Our approach can be used in both experimental and natural populations, providing a widely practicable means of expanding our understanding of MGEs.</description><subject>Animals</subject><subject>Animals, Newborn</subject><subject>Behavior</subject><subject>Cattle</subject><subject>Female</subject><subject>Genetic engineering</subject><subject>Genomes</subject><subject>Growth and Development - genetics</subject><subject>Influence</subject><subject>Investigations</subject><subject>Linear Models</subject><subject>Male</subject><subject>Metabolic disorders</subject><subject>Mice</subject><subject>Milk</subject><subject>Models, Genetic</subject><subject>Mothers</subject><subject>Phenotype</subject><subject>Quantitative Trait Loci - genetics</subject><issn>1943-2631</issn><issn>0016-6731</issn><issn>1943-2631</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><recordid>eNpdUcFO3DAQtSpQobRfUKmyuPS0i52Jk_iCVNEWkJC4tGfL8Y6DUWIH2wvqof9er3YXKAfLY82b9974EfKZsyUXUJ8N6DE7k5ac8yUHJiR_R465rGFRNcAPXtVH5ENK94yxRoruPTmqeCdZC_KY_P3uEvqs_TA6P9A5otdZj1T7FZ1DytvXpDNGX4qdJkVr0eREIz6iHhOdMSaXcmF6odhjgqfB2jTHjcAQw1O-o87TyRn8SA5tGcdPu_uE_P7549fF1eLm9vL64tvNwtTA88I0QvTltBxAWtF3AMxUXduj5QbB8tZ2otUWSqPGFsuSdrWS3HRc9lb3cELOt7zzup9wZYrPqEdVLE06_lFBO_V_x7s7NYRHBVWRFG0h-LojiOFhjSmrySWD46g9hnVSktVVVYumK8jTN8j7sN783QbUVsCariog2IJMDClFtM9WOFObcNU-XFXCVdtwy9SX11s8z-zThH9ORKaH</recordid><startdate>201111</startdate><enddate>201111</enddate><creator>Wolf, Jason B</creator><creator>Leamy, Larry J</creator><creator>Roseman, Charles C</creator><creator>Cheverud, James M</creator><general>Genetics Society of America</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>4T-</scope><scope>4U-</scope><scope>7QP</scope><scope>7SS</scope><scope>7TK</scope><scope>7TM</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>88I</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>HCIFZ</scope><scope>K9-</scope><scope>K9.</scope><scope>LK8</scope><scope>M0K</scope><scope>M0R</scope><scope>M0S</scope><scope>M1P</scope><scope>M2O</scope><scope>M2P</scope><scope>M7N</scope><scope>M7P</scope><scope>MBDVC</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>201111</creationdate><title>Disentangling prenatal and postnatal maternal genetic effects reveals persistent prenatal effects on offspring growth in mice</title><author>Wolf, Jason B ; Leamy, Larry J ; Roseman, Charles C ; Cheverud, James M</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c431t-c655b65571339f5b8330c287bef1ce3f17f857af38334e7e958fdd91c819bfab3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Animals</topic><topic>Animals, Newborn</topic><topic>Behavior</topic><topic>Cattle</topic><topic>Female</topic><topic>Genetic engineering</topic><topic>Genomes</topic><topic>Growth and Development - genetics</topic><topic>Influence</topic><topic>Investigations</topic><topic>Linear Models</topic><topic>Male</topic><topic>Metabolic disorders</topic><topic>Mice</topic><topic>Milk</topic><topic>Models, Genetic</topic><topic>Mothers</topic><topic>Phenotype</topic><topic>Quantitative Trait Loci - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wolf, Jason B</creatorcontrib><creatorcontrib>Leamy, Larry J</creatorcontrib><creatorcontrib>Roseman, Charles C</creatorcontrib><creatorcontrib>Cheverud, James M</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Docstoc</collection><collection>University Readers</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Agricultural Science Collection</collection><collection>ProQuest Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Science Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Research Library (Alumni Edition)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>AUTh Library subscriptions: ProQuest Central</collection><collection>ProQuest Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>Research Library Prep</collection><collection>SciTech Premium Collection</collection><collection>Consumer Health Database</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biological Sciences</collection><collection>Agriculture Science Database</collection><collection>Consumer Health Database</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>ProQuest research library</collection><collection>Science Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>ProQuest Biological Science Journals</collection><collection>Research Library (Corporate)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>ProQuest Central Basic</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Genetics (Austin)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wolf, Jason B</au><au>Leamy, Larry J</au><au>Roseman, Charles C</au><au>Cheverud, James M</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Disentangling prenatal and postnatal maternal genetic effects reveals persistent prenatal effects on offspring growth in mice</atitle><jtitle>Genetics (Austin)</jtitle><addtitle>Genetics</addtitle><date>2011-11</date><risdate>2011</risdate><volume>189</volume><issue>3</issue><spage>1069</spage><epage>1082</epage><pages>1069-1082</pages><issn>1943-2631</issn><issn>0016-6731</issn><eissn>1943-2631</eissn><coden>GENTAE</coden><abstract>Mothers are often the most important determinant of traits expressed by their offspring. 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MGEs contributed more to variation in body weight than the direct effects of the offsprings' own genotypes until mice reached adulthood, but continued to represent a major component of variation through adulthood. Prenatal effects always contributed more variation than postnatal effects, especially for those effects that persisted into adulthood. These results suggest that MGEs may be an important component of genetic architecture that is generally overlooked in studies focused on direct mapping from genotype to phenotype. Our approach can be used in both experimental and natural populations, providing a widely practicable means of expanding our understanding of MGEs.</abstract><cop>United States</cop><pub>Genetics Society of America</pub><pmid>21890739</pmid><doi>10.1534/genetics.111.130591</doi><tpages>14</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Animals Animals, Newborn Behavior Cattle Female Genetic engineering Genomes Growth and Development - genetics Influence Investigations Linear Models Male Metabolic disorders Mice Milk Models, Genetic Mothers Phenotype Quantitative Trait Loci - genetics |
title | Disentangling prenatal and postnatal maternal genetic effects reveals persistent prenatal effects on offspring growth in mice |
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