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Lifetime reproductive success is maximized with optimal major histocompatibility complex diversity.

Kalbe M, Eizaguirre C, Dankert I, Reusch TB, Sommerfeld RD, Wegner KM, Milinski M - Proc. Biol. Sci. (2009)

Bottom Line: However, what counts ultimately is the lifetime reproductive success (LRS).Both males and females with an intermediate MHC class IIB variant number had the highest LRS.The mechanistic link of MHC diversity and LRS differed between the sexes: in females, we found evidence for a trade-off between number of eggs and immunocompentence, whereas in males this correlation was concealed by different timing strategies of reproduction.

View Article: PubMed Central - PubMed

Affiliation: Department of Evolutionary Ecology, Max Planck Institute for Evolutionary Biology, August-Thienemann-Strasse 2, 24306 Ploen, Germany. kalbe@evolbio.mpg.de

ABSTRACT
Individual diversity at the major histocompatibility complex (MHC) is predicted to be optimal at intermediate rather than at maximal levels. We showed previously in sticklebacks that an intermediate MHC diversity is predominant in natural populations and provides maximal resistance in experimental multiple parasite infections in the laboratory. However, what counts ultimately is the lifetime reproductive success (LRS). Here, we measured LRS of six laboratory-bred sib-groups-to minimize the influence of non-MHC genes-three-spined sticklebacks (Gasterosteus aculeatus) during their entire breeding period, each in a seminatural enclosure in the lake of their parents, where they were exposed to the natural spectrum of parasites. We collected developing clutches at regular intervals and determined parenthood for a representative number of eggs (2279 in total) per clutch with 18 microsatellites. Both males and females with an intermediate MHC class IIB variant number had the highest LRS. The mechanistic link of MHC diversity and LRS differed between the sexes: in females, we found evidence for a trade-off between number of eggs and immunocompentence, whereas in males this correlation was concealed by different timing strategies of reproduction.

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Graph combining the female LRS (shown as representative number of eggs) and SSI as a function of MHC II B diversity. Females with an intermediate MHC II B diversity having the highest reproductive success are shown by black circles (neggs=38.38+4.514nMHCIIB−11.98(nMHCIIB−6.481)2, F2,26=4.63, p=0.02). Females with an intermediate MHC II B diversity having the lowest SSI, representing a better immunocompetence status, are shown by grey circles (SSI=−0.193+0.02nMHCIIB+0.057(nMHCIIB−6.536)2, F2,26=6.698, p=0.004).
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fig3: Graph combining the female LRS (shown as representative number of eggs) and SSI as a function of MHC II B diversity. Females with an intermediate MHC II B diversity having the highest reproductive success are shown by black circles (neggs=38.38+4.514nMHCIIB−11.98(nMHCIIB−6.481)2, F2,26=4.63, p=0.02). Females with an intermediate MHC II B diversity having the lowest SSI, representing a better immunocompetence status, are shown by grey circles (SSI=−0.193+0.02nMHCIIB+0.057(nMHCIIB−6.536)2, F2,26=6.698, p=0.004).

Mentions: The SSI, an indicator for immune activation, was different among enclosures (F5,51=7.96, p<0.0001), and between the sexes with females showing higher values (F1,51=6.87, p=0.012). Owing to sex differences, we split the dataset and correlated SSI with an individual MHC diversity for each sex separately. Male SSI did not show a significant relationship with MHC diversity (linear, t1,25=−1.30, p=0.206; quadratic, t1,25=−1.93, p=0.083). Females with an intermediate number of MHC variants had the lowest SSI (figure 3; quadratic, t1,28=3.41, p=0.002; linear, t1,28=1.28, p=0.212; table 1, b). Moreover, SSI correlated with the total egg number per individual for females (directed test, t1,28=−1.84, p=0.049) but not for males (directed test, t1,25=0.88, p=0.242). Since spleen size is commonly used as a diagnostic tool of the immune system, this result suggests a trade-off between reproduction and immune function only in females.


Lifetime reproductive success is maximized with optimal major histocompatibility complex diversity.

Kalbe M, Eizaguirre C, Dankert I, Reusch TB, Sommerfeld RD, Wegner KM, Milinski M - Proc. Biol. Sci. (2009)

Graph combining the female LRS (shown as representative number of eggs) and SSI as a function of MHC II B diversity. Females with an intermediate MHC II B diversity having the highest reproductive success are shown by black circles (neggs=38.38+4.514nMHCIIB−11.98(nMHCIIB−6.481)2, F2,26=4.63, p=0.02). Females with an intermediate MHC II B diversity having the lowest SSI, representing a better immunocompetence status, are shown by grey circles (SSI=−0.193+0.02nMHCIIB+0.057(nMHCIIB−6.536)2, F2,26=6.698, p=0.004).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2664370&req=5

fig3: Graph combining the female LRS (shown as representative number of eggs) and SSI as a function of MHC II B diversity. Females with an intermediate MHC II B diversity having the highest reproductive success are shown by black circles (neggs=38.38+4.514nMHCIIB−11.98(nMHCIIB−6.481)2, F2,26=4.63, p=0.02). Females with an intermediate MHC II B diversity having the lowest SSI, representing a better immunocompetence status, are shown by grey circles (SSI=−0.193+0.02nMHCIIB+0.057(nMHCIIB−6.536)2, F2,26=6.698, p=0.004).
Mentions: The SSI, an indicator for immune activation, was different among enclosures (F5,51=7.96, p<0.0001), and between the sexes with females showing higher values (F1,51=6.87, p=0.012). Owing to sex differences, we split the dataset and correlated SSI with an individual MHC diversity for each sex separately. Male SSI did not show a significant relationship with MHC diversity (linear, t1,25=−1.30, p=0.206; quadratic, t1,25=−1.93, p=0.083). Females with an intermediate number of MHC variants had the lowest SSI (figure 3; quadratic, t1,28=3.41, p=0.002; linear, t1,28=1.28, p=0.212; table 1, b). Moreover, SSI correlated with the total egg number per individual for females (directed test, t1,28=−1.84, p=0.049) but not for males (directed test, t1,25=0.88, p=0.242). Since spleen size is commonly used as a diagnostic tool of the immune system, this result suggests a trade-off between reproduction and immune function only in females.

Bottom Line: However, what counts ultimately is the lifetime reproductive success (LRS).Both males and females with an intermediate MHC class IIB variant number had the highest LRS.The mechanistic link of MHC diversity and LRS differed between the sexes: in females, we found evidence for a trade-off between number of eggs and immunocompentence, whereas in males this correlation was concealed by different timing strategies of reproduction.

View Article: PubMed Central - PubMed

Affiliation: Department of Evolutionary Ecology, Max Planck Institute for Evolutionary Biology, August-Thienemann-Strasse 2, 24306 Ploen, Germany. kalbe@evolbio.mpg.de

ABSTRACT
Individual diversity at the major histocompatibility complex (MHC) is predicted to be optimal at intermediate rather than at maximal levels. We showed previously in sticklebacks that an intermediate MHC diversity is predominant in natural populations and provides maximal resistance in experimental multiple parasite infections in the laboratory. However, what counts ultimately is the lifetime reproductive success (LRS). Here, we measured LRS of six laboratory-bred sib-groups-to minimize the influence of non-MHC genes-three-spined sticklebacks (Gasterosteus aculeatus) during their entire breeding period, each in a seminatural enclosure in the lake of their parents, where they were exposed to the natural spectrum of parasites. We collected developing clutches at regular intervals and determined parenthood for a representative number of eggs (2279 in total) per clutch with 18 microsatellites. Both males and females with an intermediate MHC class IIB variant number had the highest LRS. The mechanistic link of MHC diversity and LRS differed between the sexes: in females, we found evidence for a trade-off between number of eggs and immunocompentence, whereas in males this correlation was concealed by different timing strategies of reproduction.

Show MeSH
Related in: MedlinePlus