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European Journal of Human Genetics (2000) 8, 119–124

© 2000 Macmillan Publishers Ltd All rights reserved 1018–4813/00 $15.00 www.nature.com/ejhg

ARTICLE

A robust test for assortative mating

Em m an uelle Ge´n in 1, Carole Ober2, Lowell Weitkam p3 an d Glen ys Th om son 1

2

1Department of Integrative Biology, University of California, Berkeley, CA, USA; Department of Human Genetics,

3

University of Chicago, Chicago, IL, USA; Department of Psychiatry and Division of Genetics, University of Rochester Medical Center, Rochester, NY, USA

Testing for random mating in human populations is difficult due to confounding factors such as ethnic preference and population stratification. With HLA, the high level of polymorphism is an additional problem since it is rare for couples to share the same haplotype. Focus on an ethnically homogeneous population, where levels of polymorphism at HLA loci are more limited, may provide the best situation in which to detect non-random mating. However, such populations are often genetic isolates where there may be inbreeding to an extent that is difficult to quantify and account for. We have developed a test for random mating at a multiallelic locus that is robust to stratification and inbreeding. This test relies on the availability of genotypic information from the parents of both spouses. The focus of the test is on families where there is allele sharing between the parents of both spouses, so that potential spouses could share an allele. Denoting the shared allele at the locus of interest by A, then under the assumption of random mating, heterozygous parents AX should transmit allele A equally as frequently as allele X to their offspring. When there is positive (negative) assortative mating, A will be transmitted more (less) often than X. The power of the test has been computed in a number of situations. Data on high resolution HLA haplotypes from the Hutterite population were reinvestigated by the proposed test. The test detects significant negative assortative mating when the parental origin of the shared haplotype is taken into account. European Journal of Human Genetics (2000) 8, 119–124.

Keywords: assortative mating; HLA; Hutterites; power; robustness; inbreeding; admixture

Introduction

leukocyte an tigen s (HLA) is th e very h igh level of polym orph ism in th is region th at lowers th e expectation of fin din g spouses sh arin g an iden tical allele or h aplotype. It h as th erefore been suggested th at studies of m ate ch oice in h um an s sh ould focus on eth n ically h om ogen eous population s, wh ere levels of polym orph ism at HLA loci is m ore lim ited. However, such population s are often gen etic isolates in wh ich th ere m ay be con siderable in breedin g or, altern atively, avoidan ce of m atin g with close relatives to an exten t th at is difficult to quan tify an d accoun t for. Th e purpose of th is study is to propose a test for assortative m atin g th at is n ot sen sitive to stratification an d/or in breedin g. Th is test relies on th e availability of gen otypic in form ation for paren ts of both spouses. Th e power of th e test is com puted for differen t m odels of positive an d n egative assortative m atin g an d allowin g for differen t types of relation sh ips between th e spouses. Th e properties of th e test are com pared to th ose of on e com m on ly used test of assortative m atin g based on th e distribution of th e n um ber of alleles sh ared by spouses.4–6
Mate ch oice in an im al an d h um an population s h as been th e subject of m an y in vestigation s. Assortative m atin g h as lon g been recogn ized in h um an s for ch aracteristics such as stature an d con gen ital deafn ess,1 wh ich in volve both gen etic an d en viron m en tal factors. Studies in m ice h ave im plicated gen es from th e m ajor h istocom patibility com plex (MHC) in m ate ch oice; fem ale m ice gen erally prefer m atin g with m ales differen t from th em selves for gen es in th e H2 region .2 However, attem pts to test for an effect of HLA on m ate ch oice in h um an s h ave led to equivocal con clusion s.3–6 Con foun din g factors such as eth n ic preferen ce an d population stratification m ake testin g of ran dom m atin g in h um an population s difficult. An oth er problem specific to h um an

Correspondence: Emmanuelle Ge´nin, INSERM U535, Baˆ timent INSERM Gregory Pincus, secteur marron, porte 15, 80 rue du Ge´ne´ral Leclerc, 94276 Le Kremlin Biceˆ tre Cedex. Tel: + 33 1 49 59 53 30; Fax: + 33 1 49 59 53 31; E-mail: [email protected] Received 7 June 1999; revised 7 September 1999; accepted 23 September 1999

Testing for assortative mating

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Recen tly, two studies in h um an isolates h ave been publish ed,5,6 Th e first, in th e Hutterite population , sh owed eviden ce of n egative assortative m atin g for HLA: spouses m atch ed less often for HLA h aplotypes th an expected.5 Th is effect was n ot foun d wh en each locus was con sidered in dividually, suggestin g a h aplotype effect.7 Th e secon d study, in South Am erin dian tribes, sh owed n o deviation from ran dom m atin g wh en an alyzin g each locus separately. In both an alyses, assortative m atin g was tested by com parin g th e observed distribution of alleles or h aplotypes sh ared by spouses to th e on e expected un der ran dom m atin g an d th e sign ifican ce was depen den t on som e h ypoth eses regardin g th e structure of th e population . In th is paper, we rean alyze th e Hutterite data of Ober et al5 with th e n ew test we h ave proposed, wh ich does n ot depen d on an y h ypoth eses regardin g th e population structure. wh ere in form ative paren ts h ave tran sm itted th e sh ared allele Ai to th eir offsprin g (on e of th e spouses in gen eration G1). Th e statistic M defin ed by:

4(T – N/2)2

M =
N

is distributed as a ch i-square with on e degree of freedom un der H0. Th e test we propose is based on th is statistic an d will be called th e M test. Depen din g on th e structure of th e fam ily, th e n um ber of in form ative pairs an d in form ative paren ts m ay vary (see Table 1). Special atten tion is drawn to th e case of fam ilies wh ere on e paren t sh ares on e allele in com m on with both paren ts of h is ch ild’s in -laws, th at is fam ilies in wh ich th e paren ts of th e first spouse are AiAj, AkAl an d th e paren ts of th e secon d spouse are AiAr, AjAs. In th ese fam ilies, on ly th e paren ts of th e secon d spouse sh ould be con sidered as in form ative with th e sh ared allele bein g respectively Ai an d Aj. Th e con sequen ce is th at th e test requires at least th ree alleles be presen t in th e fam ily. Th erefore it can n ot be used with biallelic m arkers. In deed, with biallelic m arkers, h eterozygous paren ts can on ly sh are alleles with both paren ts of th eir ch ild’s in -laws.

Material and methods

Description of th e m atin g test

Th e robust test we h ave developed relies on th e availability of gen otypic in form ation for th e paren ts (gen eration G0) of both spouses (gen eration G1), an d focuses on ly on fam ilies wh ere th e paren ts sh are an allele, called Ai, at th e test locus un der study (see Table 1). Th e pair of paren ts sh arin g a com m on allele is called an in form ative pair. Un der th e assum ption of ran dom m atin g at gen eration G1, paren ts th at are h eterozygous AiAj tran sm it allele Ai as often as allele Aj to th eir offsprin g. If th e sh ared allele Ai is tran sm itted m ore often , it m ean s th at in gen eration G1, th ere was positive assortative m atin g with respect to th e locus un der study or a locus in lin kage disequilibrium with th at locus (see discussion ). Con versely, if Ai is tran sm itted less often th an Aj, it m ean s th at in gen eration G1, th ere was n egative assortative m atin g at th at locus.

Statistical properties of th e M test com pared with th e IBS test

Th e statistical properties of th e M test (robustn ess an d power) h ave been studied by sim ulation s. A com parison is perform ed with th e classically used iden tical by state (IBS) test.4–6

Description of the IBS test Th e IBS test is also a ch i-square

test th at com pares th e observed distribution of spouses sh arin g 0, 1 or 2 IBS alleles to th e distribution expected un der ran dom m atin g (P0, P1, P2). To avoid an y assum ption regardin g th e m atin g pattern in th e paren tal gen eration , Hedrick8 proposed estim atin g P0, P1 an d P2 from th e data by
Let N be th e n um ber of h eterozygous paren ts AiAj in in form ative pairs (we will refer to th ese paren ts as in form ative paren ts in th e followin g). Let T be th e n um ber of cases

Table 1 Families considered in the analysis

No. of informative pairs per family
No. of informative

  • parents
  • Type
  • Parents of 1st spouse
  • Parents of 2nd spouse

  • 1
  • AA A A
  • AAm A A
  • i ≠ j, k, l

m, r, s ≠ i, k, l i ≠ k, l
112
214

  • i
  • j
  • k
  • l
  • i
  • r
  • s

23

  • AA A A
  • AAm A A

  • i
  • i
  • k
  • l
  • i
  • r
  • s

m, r, s ≠ i, k, l i ≠ j, k, l l ≠ k

  • AA A A
  • AAm A A

  • i
  • j
  • k
  • l
  • i
  • k
  • r

m, r ≠ i, j, k, l i ≠ k, l
4

56

  • AA A A
  • AAm A A
  • 2

22
322

  • i
  • i
  • k
  • l
  • i
  • k
  • r

l ≠ k m, r ≠ i, k, l i ≠ k, m

  • AA A A
  • AAm A A

  • i
  • i
  • k
  • k
  • i
  • k
  • r

m ≠ k r ≠ i, j, k i ≠ j, k, l m, r ≠ i, j, k, l

  • AA A A
  • AAm AA

  • i
  • j
  • k
  • l
  • i
  • j
  • r

European Journal of Human Genetics
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usin g th e observed fem ale an d m ale gen otypic frequen cies in m atin g pairs from th e population .
Th ese param eters clearly h ave an in fluen ce: 1. on th e probability of recruitin g fam ilies with in form ative pairs, an d 2. on th e power of th e M test to detect assortative m atin g.

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    208 Вивчення популяційних систем зелених жаб (Rana esculenta complex) в Харківській … УДК: 597.851(477.54) ИЗУЧЕНИЕ ПОПУЛЯЦИОННЫХ СИСТЕМ ЗЕЛЕНЫХ ЛЯГУШЕК (RANA ESCULENTA COMPLEX) В ХАРЬКОВСКОЙ ОБЛАСТИ: ИСТОРИЯ, СОВРЕМЕННОЕ СОСТОЯНИЕ И ПЕРСПЕКТИВЫ Д.А.Шабанов, А.И.Зиненко, А.В.Коршунов, М.А.Кравченко, Г.А.Мазепа Харьковский национальный университет имени В.Н.Каразина (Харьков, Украина) В статье дан обзор среднеевропейских зеленых лягушек (Rana esculenta complex). Описано характерное для их межвидовых гибридов мероклональное наследование (передача одного из геномов без рекомбинации). Описаны основные методы исследования этого явления, а также история изучения зеленых лягушек на территории Харьковской области. В Харьковской области зарегистрированы разные типы популяционных систем зеленых лягушек, в том числе включающие ди- и полиплоидные гибриды. Высказано предположение, что состав популяционных систем зеленых лягушек отражает результат их локальной эволюции и частотно-зависимого отбора гибридных линий, производящих разные типы гамет. Предложена схема, описывающая возможные преобразования популяционных систем в ходе их эволюции. Сформулированы перспективные направления дальнейших исследований разнообразия зеленых лягушек в Харьковской области. Ключевые слова: Rana esculenta complex, триплоиды, тетраплоиды, гибридогенез, мероклональное наследование, популяционные системы, Харьковская область. Мероклональное наследование у Rana esculenta В состав комплекса среднеевропейских зеленых лягушек (Rana esculenta complex) входят три основные формы.
  • The Evolutionary Significance of Polyploidy Yves Van De Peer1,2,3,4, Eshchar Mizrachi4,5, and Kathleen Marchal1,3,5,6

    The Evolutionary Significance of Polyploidy Yves Van De Peer1,2,3,4, Eshchar Mizrachi4,5, and Kathleen Marchal1,3,5,6

    This is a post-print of an article published in Nature Reviews Genetics. The final authenticated version is available online at: https://doi.org/10.1038/nrg.2017.26 The evolutionary significance of polyploidy Yves Van de Peer1,2,3,4, Eshchar Mizrachi4,5, and Kathleen Marchal1,3,5,6 1 Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 927, B-9052 Ghent, Belgium. 2 VIB-UGent Center for Plant Systems Biology, VIB, Technologiepark 927, B-9052 Ghent, Belgium 3 Bioinformatics Institute Ghent, Ghent University, Technologiepark 927, B-9052 Ghent, Belgium 4 Genomics Research Institute (GRI), University of Pretoria, Private Bag X20, Pretoria, 0028, South Africa 5 Department of Genetics, Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Private Bag X20, Pretoria, 0028, South Africa 6 Department of Information Technology, IDLab, imec, Ghent University, B-9052 Ghent, Belgium Correspondence to Y. V. d. P. [email protected] Abstract Polyploidy, or the duplication of entire genomes, has been observed in both somatic and germ cells, and in both prokaryotic and eukaryotic organisms. Although the consequences of polyploidization are complex and variable, and seem to differ greatly between systems (clonal and non-clonal) and species, there is growing evidence that polyploidization correlates with environmental change or stress. Consequently, although often considered an evolutionary dead end, the short-term adaptive potential of polyploidization is increasingly being acknowledged. Furthermore, once established, the unique retention profile of duplicated genes following whole-genome duplication might explain important longer-term key evolutionary transitions and a general increase in biological complexity. Introduction Polyploid species (BOX 1) have been known for a long time.
  • Mechanisms of Assortative Mating in Speciation

    Mechanisms of Assortative Mating in Speciation

    Mechanisms of Assortative Mating in Speciation with Gene Flow: Connecting Theory and Empirical Research Michael Kopp, Maria Servedio, Tamra Mendelson, Rebecca Safran, Rafael Rodríguez, Mark Hauber, Elizabeth Scordato, Laurel Symes, Christopher Balakrishnan, David Zonana, et al. To cite this version: Michael Kopp, Maria Servedio, Tamra Mendelson, Rebecca Safran, Rafael Rodríguez, et al.. Mech- anisms of Assortative Mating in Speciation with Gene Flow: Connecting Theory and Empirical Re- search. American Naturalist, University of Chicago Press, 2018, 191 (1), pp.1-20. 10.1086/694889. hal-02013886 HAL Id: hal-02013886 https://hal.archives-ouvertes.fr/hal-02013886 Submitted on 2 May 2019 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. vol. 191, no. 1 the american naturalist january 2018 Synthesis Mechanisms of Assortative Mating in Speciation with Gene Flow: Connecting Theory and Empirical Research Michael Kopp,1,*,† Maria R. Servedio,2,* Tamra C. Mendelson,3 Rebecca J. Safran,4 Rafael L. Rodríguez,5 Mark E. Hauber,6 Elizabeth C. Scordato,4 Laurel B. Symes,7 Christopher N. Balakrishnan,8 David M. Zonana,4 and G. Sander van Doorn9 1. Aix Marseille Université, CNRS, Centrale Marseille, I2M, 3 Place Victor Hugo, 13331 Marseille Cedex 3, France; 2.