Supporting information about data
This document includes three sections (1) Data bibliography (2) Details of data extraction and
effect size averaging, and (3) List of relevant papers excluded from the present study.
Data bibliography:
The references below are those from which data were extracted to calculate effect sizes for metaanalyses. Actual effect sizes and associated information, such as moderator variables and species
names can be found in the supporting electronic data files.
Aeschlimann PB, Häberli MA, Reusch TBH, Boehm T, Milinski M (2003) Female sticklebacks
Gasterosteus aculeatus use self-reference to optimize MHC allele number during mate selection.
Behavioral Ecology and Sociobiology, 54, 119–126.
Agbali M, Reichard M, Bryjová A, Bryja J, Smith C (2010) Mate choice for nonadditive genetic benefits
correlate with MHC dissimilarity in the rose bitterling (Rhodeus ocellatus). Evolution, 64, 1683–1696.
Bahr A, Sommer S, Mattle B, Wilson AB (2012) Mutual mate choice in the potbellied seahorse
(Hippocampus abdominalis). Behavioral Ecology, 23, 869–878.
Bonneaud C, Chastel O, Federici P, Westerdahl H, Sorci G (2006) Complex MHC-based mate choice in a
wild passerine. Proceedings of the Royal Society B: Biological Sciences, 273, 1111–1116.
Bos DH, Williams RN, Gopurenko D, Bulut Z, Dewoody JA (2009) Condition-dependent mate choice
and a reproductive disadvantage for MHC-divergent male tiger salamanders. Molecular Ecology, 18,
3307–3315.
Cutrera AP, Fanjul MS, Zenuto RR (2012) Females prefer good genes: MHC-associated mate choice in
wild and captive tuco-tucos. Animal Behaviour, 83, 847–856.
Egid K, Brown JL (1989) The major histocompatibility complex and female mating preferences in mice.
Animal Behaviour, 38, 548–549.
Ehman KD, Scott ME (2001) Urinary odour preferences of MHC congenic female mice, Mus domesticus:
implications for kin recognition and detection of parasitized males. Animal Behaviour, 62, 781–789.
Eizaguirre C, Yeates SE, Lenz TL, Kalbe M, Milinski M (2009) MHC-based mate choice combines good
genes and maintenance of MHC polymorphism. Molecular Ecology, 18, 3316–3329.
Ekblom R, Sæther SA, Grahn M et al. (2004) Major histocompatibility complex variation and mate
choice in a lekking bird, the great snipe (Gallinago media). Molecular Ecology, 13, 3821–3828.
Eklund A, Egid K, Brown JL (1991) The major histocompatibility complex and mating preferences of
male mice. Animal Behaviour, 42, 693–694.
Evans ML, Dionne M, Miller KM, Bernatchez L (2012a) Mate choice for major histocompatibility
complex genetic divergence as a bet-hedging strategy in the Atlantic salmon (Salmo salar). Proceedings
of the Royal Society B: Biological Sciences, 279, 379–386.
Evans ML, Neff BD, Heath DD (2012b) Behavioural and genetic analyses of mate choice and
reproductive success in two Chinook salmon populations. Canadian Journal of Fisheries and Aquatic
Sciences, 70, 263–270.
Freeman-Gallant CR, Meguerdichian M, Wheelwright NT, Sollecito SV (2003) Social pairing and female
mating fidelity predicted by restriction fragment length polymorphism similarity at the major
histocompatibility complex in a songbird. Molecular Ecology, 12, 3077–3083.
Gillingham MAF, Richardson DS, Løvlie H et al. (2009) Cryptic preference for MHC-dissimilar females
in male red junglefowl, Gallus gallus. Proceedings of the Royal Society B: Biological Sciences, 276,
1083–1092.
Griggio M, Biard C, Penn DJ, Hoi H (2011) Female house sparrows “count on” male genes: experimental
evidence for MHC-dependent mate preference in birds. BMC Evolutionary Biology, 11, 44.
Huchard E, Baniel A, Schliehe-Diecks S, Kappeler PM (2013) MHC-disassortative mate choice and
inbreeding avoidance in a solitary primate. Molecular Ecology, 22, 4071–4086.
Huchard E, Knapp LA, Wang J, Raymond M, Cowlishaw G (2010) MHC, mate choice and heterozygote
advantage in a wild social primate. Molecular Ecology, 19, 2545–2561.
Jäger I, Eizaguirre C, Griffiths SW et al. (2007) Individual MHC class I and MHC class IIB diversities
are associated with male and female reproductive traits in the three-spined stickleback. Journal of
Evolutionary Biology, 20, 2005–2015.
Kalbe M, Eizaguirre C, Dankert I et al. (2009) Lifetime reproductive success is maximized with optimal
major histocompatibility complex diversity. Proceedings of the Royal Society B: Biological Sciences, 276,
925–934.
Knafler GJ, Clark JA, Boersma PD, Bouzat JL (2012) MHC diversity and mate choice in the magellanic
penguin, Spheniscus magellanicus. Journal of Heredity, 103, 759–768.
Landry C, Garant D, Duchesne P, Bernatchez L (2001) “Good genes as heterozygosity”: the major
histocompatibility complex and mate choice in Atlantic salmon (Salmo salar). Proceedings of the Royal
Society B: Biological Sciences, 268, 1279–1285.
Løvlie H, Gillingham MAF, Worley K, Pizzari T, Richardson DS (2013) Cryptic female choice favours
sperm from major histocompatibility complex-dissimilar males. Proceedings of the Royal Society B:
Biological Sciences, 280, 20131296.
McCairns RJS, Bourget S, Bernatchez L (2011) Putative causes and consequences of MHC variation
within and between locally adapted stickleback demes. Molecular Ecology, 20, 486–502.
Miller HC, Moore JA, Nelson NJ, Daugherty CH (2009) Influence of major histocompatibility complex
genotype on mating success in a free-ranging reptile population. Proceedings of the Royal Society B:
Biological Sciences, 276, 1695–1704.
Nelson NJ, Daugherty CH (2009) Influence of major histocompatibility complex genotype on mating
success in a free-ranging reptile population. Proceedings of the Royal Society B: Biological Sciences, 276,
1695–1704.
Olsson M, Madsen T, Nordby J et al. (2003) Major histocompatibility complex and mate choice in sand
lizards. Proceedings of the Royal Society B: Biological Sciences, 270, S254–S256.
Olsson M, Madsen T, Ujvari B, Wapstra E (2004) Fecundity and MHC affects ejaculation tactics and
paternity bias in sand lizards. Evolution, 58, 906–909.
Paterson S, Pemberton JM (1997) No evidence for major histocompatibility complex-dependent mating
patterns in a free-living ruminant population. Proceedings of the Royal Society B: Biological Sciences,
264, 1813–1819.
Penn D, Potts W (1998) MHC-disassortative mating preferences reversed by cross-fostering. Proceedings
of the Royal Society B: Biological Sciences, 265, 1299–1306.
Potts WK, Manning CJ, Wakeland EK (1991) Mating patterns in seminatural populations of mice
influenced by MHC genotype. Nature, 352, 619–621.
Radwan J, Tkacz A, Kloch A (2008) MHC and preferences for male odour in the bank vole. Ethology,
114, 827–833.
Reusch TB, Häberli MA, Aeschlimann PB, Milinski M (2001) Female sticklebacks count alleles in a
strategy of sexual selection explaining MHC polymorphism. Nature, 414, 300–302.
Richardson DS, Komdeur J, Burke T, Schantz T von (2005) MHC-based patterns of social and extra-pair
mate choice in the Seychelles warbler. Proceedings of the Royal Society B: Biological Sciences, 272,
759–767.
Roberts SC, Gosling LM (2003) Genetic similarity and quality interact in mate choice decisions by
female mice. Nature Genetics, 35, 103–106.
Sauermann U, Nürnberg P, Bercovitch F et al. (2001) Increased reproductive success of MHC class II
heterozygous males among free-ranging rhesus macaques. Human Genetics, 108, 249–254.
Schwensow N, Fietz J, Dausmann K, Sommer S (2008) MHC-associated mating strategies and the
importance of overall genetic diversity in an obligate pair-living primate. Evolutionary Ecology, 22, 617–
636.
Setchell JM, Charpentier MJE, Abbott KM, Wickings EJ, Knapp LA (2010) Opposites attract: MHCassociated mate choice in a polygynous primate. Journal of Evolutionary Biology, 23, 136–148.
Sherborne AL, Thom MD, Paterson S et al. (2007) The genetic basis of inbreeding avoidance in house
mice. Current Biology, 17, 2061–2066.
Skarstein F, Folstad I, Liljedal S, Grahn M (2005) MHC and fertilization success in the Arctic charr
(Salvelinus alpinus). Behavioral Ecology and Sociobiology, 57, 374–380.
Sommer S (2005) Major histocompatibility complex and mate choice in a monogamous rodent.
Behavioral Ecology and Sociobiology, 58, 181–189.
Strandh M, Westerdahl H, Pontarp M et al. (2012) Major histocompatibility complex class II
compatibility, but not class I, predicts mate choice in a bird with highly developed olfaction. Proceedings
of the Royal Society B: Biological Sciences, 279, 4457–4463.
Thom MD, Stockley P, Jury F et al. (2008) The direct assessment of genetic heterozygosity through scent
in the mouse. Current Biology, 18, 619–623.
Wedekind C, Chapuisat M, Macas E, Rülicke T (1996) Non-random fertilization in mice correlates with
the MHC and something else. Heredity, 77 ( Pt 4), 400–409.
Westerdahl H (2004) No evidence of an MHC-based female mating preference in great reed warblers.
Molecular Ecology, 13, 2465–2470.
Yamazaki K, Boyse EA, Miké V et al. (1976) Control of mating preferences in mice by genes in the
major histocompatibility complex. Journal of Experimental Medicine, 144, 1324–1335.
Yamazaki K, Yamaguchi M, Andrews PW, Peake B, Boyse EA (1978) Mating preferences of F2
segregants of crosses between MHC-congenic mouse strains. Immunogenetics, 6, 253–259.
Yeates SE, Einum S, Fleming IA et al. (2009) Atlantic salmon eggs favour sperm in competition that
have similar major histocompatibility alleles. Proceedings of the Royal Society B: Biological Sciences,
276, 559–566.
Details of data extraction and effect size averaging
Details of data extraction from papers where test statistics other than the standard effect size
were reported, or from which we calculated the average effect size from multiple test statistics
are listed below:
Publication
Details
Agbali et al. 2010
The mean effect size was calculated among different measures of
dissimilarity (i.e. dissimilarity based on 1. functional distance in
amino acid sequence, 2. phylogenetic distance in amino acid
sequence, 3. strongly positively selected sites, and 4. positively
selected sites).
Bahr et al. 2012
The weighted mean effect size was calculated among different
measures of mating preference (i.e. preference based on 1.
olfactory cues only and 2. visual and olfactory cues).
Bonneaud et al. 2006
The mean effect size for similarity was calculated between mated
vs. random and mated vs non-mated.
Cutrera et al. 2012
The weighted (for sample size) mean effect size among olfactorybased preference, confined male preference and tethered male
preference was calculated. The weighted mean effect size was
then calculated between wild and captive populations.
Ehman & Scott 2001
The proportion of time spent with MHC similar males was
compared against the null expectation of 50% and an effect size
was computed using the effect size calculator for proportional
data.
Eklund 1990
The number of males that mated with the identical-MHC females
was analysed using Chi-squared test for goodness of fit. The
weighted (for sample size) mean effect size between GAA and
CHR haplotypes was then calculated.
Evans et al. 2013
The effect size, r, was calculated from the p-value. The sample
size, and hence df for this calculation was based on the number of
chosen sex individuals (as opposed to the number of choosy sex
individuals) since the permutation tests were carried out based on
the number of chosen sex individuals. The weighted mean effect
sizes were calculated between the populations, Little Qualicum
and Quinsam.
Freeman-Gallant et al.
The number of females that mated with MHC similar males was
2003
analysed using Chi-squared test for goodness of fit. The effect
size was then calculated from the Chi-squared values. The mean
effect size was calculated between the two age groups, i.e.
yearlings and old females.
Gillingham et al. 2009
The mean effect sizes were calculated among different similarity
measures (i.e. number of alleles and number of haplotypes
shared) and simultaneous and sequential choice for both pre- and
post-copulatory choices.
Griggio et al. 2011
The proportion of time spent by focal female (i.e. a measure of
preference) was extracted from Figure 2 using GetData
(www.getdata-graph-digitizer.com). The mean effect size among
Low-High, Low-Intermediate, Intermediate-High males was then
calculated for each class (i.e. low, intermediate, and high) of
females. Then the average effect size was calculated among the
three classes of females.
Huchard et al. 2010
The mean effect sizes were calculated among different similarity
measures (i.e. number of sequence, supertype & haplotype). The
results for female reproductive success were left out as the
information on the choosing males was unavailable (hence it was
decided that the female reproductive success was not presented as
a proxy of male choice).
Data for all females were used. Three average effect sizes were
calculated from this paper. 1) The average effect size between
MHC loci for band-based dissimilarity measures; 2) The average
effect size calculated between different MHC loci (i.e. DRB &
DQB) and dissimilarity measures for sequence-based data (i.e.
mean number of amino acid differences between the 4 possible
combinations of a pair, number of amino acid differences
between the most similar haplotypes (sequences) of a pair), mean
functional distance between the 4 possible haplotypes (sequences)
combinations of a pair, functional distance between the most
similar haplotypes (sequences) of a pair; 3) The average effect
size between different MHC loci (i.e. DRB & DQB) and diversity
measures (i.e. number of amino acids that differ between the 2
haplotypes (sequences) possessed by the mate and functional
distance between the 2 haplotypes (sequences) possessed by the
mate).
The results partially overlapping with Evans et al. 2012 Proc B
were not included in the present analysis.
The average effect sizes were calculated between major and
minor loci within MHC classes. Additionally for female choice,
the effect sizes were further averaged between two measures of
cryptic preference (i.e. sperm number on eggs and ejaculate
ejection)
The total number of combined, unique PBR sequences per
potential couple was not included as it is a measure of both
diversity and dissimilarity of the chosen mate. The weighted
average between the demes and environments were calculated.
The weighted (for sample size) mean effect size between the
three different measures of preference (i.e. visit to side, time
spent and number of visits in box) was calculated.
From Table 2b, only the expressed MHC Class 2 marker (i.e.
OLADRB) and the Class 1 marker (i.e. OMHC1) were included,
Huchard et al. 2013
Landry et al. 2001
Løvlie et al. 2013
McCairns et al. 2011
Olsson et al. 2003
Paterson & Pemberton
1997
Penn & Potts 1998
Potts et al. 1991
Sauermann et al. 2001
Setchell et al. 2010
Sherborne et al. 2007
Schwensow et al. 2008
Strandh et al. 2012
since other loci were either non-expressed or flanking marker
controls. For each class, a Chi-squared test (comparing sharing 0
to 1 and 2) was conducted and the average Chi-squared value was
calculated, from which the effect size, r, was calculated.
The results from the out-fostering portion were excluded as postbirth conditioning was unique to this paper and also not the focus
of our study. The mating score was analysed using Chi-squared
test for goodness of fit. Also the number of females that mated
with MHC similar males was analysed using Chi-squared test for
goodness of fit. The effect size was then calculated from the Chisquared values.
From Table 1, a Chi-squared value was calculated from the sum
of observed and expected MHC heterozygosity / homozygosity of
9 populations. The sample size was approximated as the sum of
males involved. From Table 2, Chi-squared values were
calculated from the observed and expected MHC heterozygosity /
homozygosity of nestlings and embryos. Additionally, a Chisquared value was calculated from the average observed and
expected MHC heterozygosity / homozygosity of informative
laboratory matings. From Table 3, Chi-squared values were
calculated from the observed and expected MHC heterozygosity /
homozygosity of territorial and extra-territorial matings;
corresponding sample sizes were taken from the text. Then the
weighted average effect size was calculated between the number
of nestlings and embryos and between laboratory matings and
territorial matings.
The weighted mean effect size was calculated between wild and
captive populations.
The average effect size was calculated between band-based
dissimilarity measures (i.e. number of sequences and supertypes
difference). Likewise for diversity measures, the average effect
size was calculated between the number of sequences and number
of supertypes.
From Table S2, a Chi-squared test (comparing sharing 0 to 1 and
2) was conducted for each of the MHC related models (i.e.
number of matings, number of offspring, and offspring MHC
genotypes). Then the weighted average effect size was calculated
for the measures of reproductive success (i.e. the number of
matings and offspring).
The weighted average effect sizes were calculated between MHC
measures based on alleles and supertypes, between social fathers
and genetic fathers, and between extra-pair mating comparisons
based on ‘cuckolded social males vs non-cuckolded males’ and
‘cuckolded social males vs genetic EPY fathers’
The average effect sizes between phylogenetic and functional
Thom et al. 2008
Wedekind et al. 1996
Westerdahl 2004
Yamazaki et al. 1976
Yamazaki et al. 1978
diversity were calculated.
The weighted (for sample size) mean effect size between different
measures of preference (territory, nest and nest + male) was
calculated.
Only the overall proportion of homozygosity was used as the
main findings of the paper (i.e. the change in heterozygosity over
time was out of the scope of the present analysis).
The mean effect size for similarity was calculated between mated
vs. random and mated vs average.
Since it was unclear whether results were derived from single or
multiple experiments, only the results shown in Figure 1 were
extracted for each cross separately (results reported in Table 2
and 3 are likely to be from the same experiment). The weighted
average proportion for each cross was calculated based on the
sample size and the proportion of males that preferred MHC dissimilar females was analysed using Chi-squared test for
goodness of fit. The effect size was then calculated from the Chisquared values. Then the weighted average effect size among the
three crosses was calculated.
The proportion of preference for dissimilar mates was extracted
using GetData (www.getdata-graph-digitizer.com).The weighted
(for sample size) average dissimilarity preference for the
BALB/BALB.B strain was calculated for Figure 2 Group 2, 5,
and 6 and Figure 3 Group 2-4. Group 3 and 4 from Figure 2 were
excluded because the equivalent comparisons are not found in
Figure 3. Similarly, the weighted (for sample size) average
preference for B6/B6.H-2k strain was calculated for Group 2 from
Figure 4. In both cases Group 1 was excluded because the data
come from a previously published paper (i.e. Yamazaki et al.
1976 J Exp Med). Then the weighted average effect size among
crosses and strains was calculated.
List of excluded papers
Relevant studies excluded from the presented study and the reason for exclusion are listed below
Publication
Reasons
Beauchamp et al. 2000
Female genotypes are identical between treatments.
Beauchamp et al. 1988
Table 1 & 2, Figure 2 & 3 are from Yamazaki et al. (1976) &
(1978). In Figure 4, the genetic identity of choosy females is
unclear.
Consuegra & de Leaniz 2008 Only offspring MHC dissimilarity was reported.
Garner et al. 2010
Only offspring MHC dissimilarity was reported.
Wedekind et al. 2004
Test statistics for the association between MHC genotypes and
fertilisation are reported while no information with regard to
diversity, heterozygosity or dissimilarity is available.
Neff et al. 2008
Only offspring MHC dissimilarity was reported.
Schwensow et al. 2008
Some effect sizes (for male choice) were reported without
slopes, but the same data were used by Huchard et al. (2013)
Beauchamp GK, Curran M, Yamazaki K (2000) MHC-mediated fetal odourtypes expressed by pregnant
females influence male associative behaviour. Animal Behaviour, 60, 289–295.
Beauchamp GK, Yamazaki K, Bard J, Boyse EA (1988) Preweaning experience in the control of mating
preferences by genes in the major histocompatibility complex of the mouse. Behavior Genetics, 18, 537–
547.
Consuegra S, Leaniz CG de (2008) MHC-mediated mate choice increases parasite resistance in salmon.
Proceedings of the Royal Society B: Biological Sciences, 275, 1397–1403.
Garner SR, Bortoluzzi RN, Heath DD, Neff BD (2010) Sexual conflict inhibits female mate choice for
major histocompatibility complex dissimilarity in Chinook salmon. Proceedings of the Royal Society B:
Biological Sciences, 277, 885–894.
Neff BD, Garner SR, Heath JW, Heath DD (2008) The MHC and non-random mating in a captive
population of Chinook salmon. Heredity, 101, 175–185.
Schwensow N, Eberle M, Sommer S (2008) Compatibility counts: MHC-associated mate choice in a wild
promiscuous primate. Proceedings of the Royal Society B: Biological Sciences, 275, 555–564.
Wedekind C, Walker M, Portmann J et al. (2004) MHC-linked susceptibility to a bacterial infection, but
no MHC-linked cryptic female choice in whitefish. Journal of Evolutionary Biology, 17, 11–18.