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The impact of sex-role reversal on the diversity of the major histocompatibility complex: insights from the seahorse (Hippocampus abdominalis).

Bahr A, Wilson AB - BMC Evol. Biol. (2011)

Bottom Line: The MHIIβ locus of the seahorse exhibits a novel expression domain in the male brood pouch.The high variation found at the seahorse MHIIβ gene indicates that sex-role reversed species are capable of maintaining the high MHC diversity typical in most vertebrates.Whether such species have evolved the capacity to use MH-odor cues during mate choice is presently being investigated using mate choice experiments.If this possibility can be rejected, such systems would offer an exceptional opportunity to study the effects of natural selection in isolation, providing powerful comparative models for understanding the relative importance of selective factors in shaping patterns of genetic variation.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Evolutionary Biology and Environmental Studies, University of Zurich, Winterthurerstrasse 190, 8057 Zurich, Switzerland.

ABSTRACT

Background: Both natural and sexual selection are thought to influence genetic diversity, but the study of the relative importance of these two factors on ecologically-relevant traits has traditionally focused on species with conventional sex-roles, with male-male competition and female-based mate choice. With its high variability and significance in both immune function and olfactory-mediated mate choice, the major histocompatibility complex (MHC/MH) is an ideal system in which to evaluate the relative contributions of these two selective forces to genetic diversity. Intrasexual competition and mate choice are both reversed in sex-role reversed species, and sex-related differences in the detection and use of MH-odor cues are expected to influence the intensity of sexual selection in such species. The seahorse, Hippocampus abdominalis, has an exceptionally highly developed form of male parental care, with female-female competition and male mate choice.

Results: Here, we demonstrate that the sex-role reversed seahorse has a single MH class II beta-chain gene and that the diversity of the seahorse MHIIβ locus and its pattern of variation are comparable to those detected in species with conventional sex roles. Despite the presence of only a single gene copy, intralocus MHIIβ allelic diversity in this species exceeds that observed in species with multiple copies of this locus. The MHIIβ locus of the seahorse exhibits a novel expression domain in the male brood pouch.

Conclusions: The high variation found at the seahorse MHIIβ gene indicates that sex-role reversed species are capable of maintaining the high MHC diversity typical in most vertebrates.Whether such species have evolved the capacity to use MH-odor cues during mate choice is presently being investigated using mate choice experiments. If this possibility can be rejected, such systems would offer an exceptional opportunity to study the effects of natural selection in isolation, providing powerful comparative models for understanding the relative importance of selective factors in shaping patterns of genetic variation.

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Amino acid alignment of β1-domain. MHII β1 sequences for H. abdominalis (Hiab), Homo sapiens (Hosa) and published teleost species (see methods). "S" represents positively selected sites in the seahorse as inferred from the exon 2 dataset, "B" indicates human PBS according to Brown et al. [10] and "R" reflects human PBS according to Reche and Reinherz [50]. Amino acid positions of the human MHII β1-domain are indicated below the human sequence.
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Figure 4: Amino acid alignment of β1-domain. MHII β1 sequences for H. abdominalis (Hiab), Homo sapiens (Hosa) and published teleost species (see methods). "S" represents positively selected sites in the seahorse as inferred from the exon 2 dataset, "B" indicates human PBS according to Brown et al. [10] and "R" reflects human PBS according to Reche and Reinherz [50]. Amino acid positions of the human MHII β1-domain are indicated below the human sequence.

Mentions: Sequencing of the highly-variable peptide binding region of the seahorse MHIIβ locus identified a total of 17 H. abdominalis MHII β1-domain alleles in 101 individuals (Figure 2). 86% of individuals were heterozygous for MHIIβ (87 of 101), while 14% were homozygous, consistent with Hardy-Weinberg expectations (HWE Exact Test: p = 0.08). An analysis of allelic assortment detected 4 allele combinations more frequently than expected by chance (Figure 3; Hiab-DAB-E2*03/*03 p = 0.020, *04/*05 p = 0.040, *05/*13 p = 0.029, *07/*08 p = 0.001), but none of these values remained significant after correcting for multiple comparisons (Sequential Bonferroni correction). The 17 alleles include 25 polymorphic nucleotide sites and a total of 17 amino acid differences (Figure 4). Each of the 17 alleles differs by at least one amino acid substitution (Figure 4, 5). All alleles detected in wild individuals (Hiab-DAB-E2*01, 04, 05, 09, 13, 16 and 17) were also detected in the captive-bred population. The nucleotide diversity π of the seahorse MHII β1-domain is 0.034. The dataset used for subsequent analyses contains 270 bp of exon 2 (total length: 273 bp), after omitting exon-spanning codons at the 5' and 3' ends of the exon (2 bp and 1 bp, respectively).


The impact of sex-role reversal on the diversity of the major histocompatibility complex: insights from the seahorse (Hippocampus abdominalis).

Bahr A, Wilson AB - BMC Evol. Biol. (2011)

Amino acid alignment of β1-domain. MHII β1 sequences for H. abdominalis (Hiab), Homo sapiens (Hosa) and published teleost species (see methods). "S" represents positively selected sites in the seahorse as inferred from the exon 2 dataset, "B" indicates human PBS according to Brown et al. [10] and "R" reflects human PBS according to Reche and Reinherz [50]. Amino acid positions of the human MHII β1-domain are indicated below the human sequence.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3117728&req=5

Figure 4: Amino acid alignment of β1-domain. MHII β1 sequences for H. abdominalis (Hiab), Homo sapiens (Hosa) and published teleost species (see methods). "S" represents positively selected sites in the seahorse as inferred from the exon 2 dataset, "B" indicates human PBS according to Brown et al. [10] and "R" reflects human PBS according to Reche and Reinherz [50]. Amino acid positions of the human MHII β1-domain are indicated below the human sequence.
Mentions: Sequencing of the highly-variable peptide binding region of the seahorse MHIIβ locus identified a total of 17 H. abdominalis MHII β1-domain alleles in 101 individuals (Figure 2). 86% of individuals were heterozygous for MHIIβ (87 of 101), while 14% were homozygous, consistent with Hardy-Weinberg expectations (HWE Exact Test: p = 0.08). An analysis of allelic assortment detected 4 allele combinations more frequently than expected by chance (Figure 3; Hiab-DAB-E2*03/*03 p = 0.020, *04/*05 p = 0.040, *05/*13 p = 0.029, *07/*08 p = 0.001), but none of these values remained significant after correcting for multiple comparisons (Sequential Bonferroni correction). The 17 alleles include 25 polymorphic nucleotide sites and a total of 17 amino acid differences (Figure 4). Each of the 17 alleles differs by at least one amino acid substitution (Figure 4, 5). All alleles detected in wild individuals (Hiab-DAB-E2*01, 04, 05, 09, 13, 16 and 17) were also detected in the captive-bred population. The nucleotide diversity π of the seahorse MHII β1-domain is 0.034. The dataset used for subsequent analyses contains 270 bp of exon 2 (total length: 273 bp), after omitting exon-spanning codons at the 5' and 3' ends of the exon (2 bp and 1 bp, respectively).

Bottom Line: The MHIIβ locus of the seahorse exhibits a novel expression domain in the male brood pouch.The high variation found at the seahorse MHIIβ gene indicates that sex-role reversed species are capable of maintaining the high MHC diversity typical in most vertebrates.Whether such species have evolved the capacity to use MH-odor cues during mate choice is presently being investigated using mate choice experiments.If this possibility can be rejected, such systems would offer an exceptional opportunity to study the effects of natural selection in isolation, providing powerful comparative models for understanding the relative importance of selective factors in shaping patterns of genetic variation.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Evolutionary Biology and Environmental Studies, University of Zurich, Winterthurerstrasse 190, 8057 Zurich, Switzerland.

ABSTRACT

Background: Both natural and sexual selection are thought to influence genetic diversity, but the study of the relative importance of these two factors on ecologically-relevant traits has traditionally focused on species with conventional sex-roles, with male-male competition and female-based mate choice. With its high variability and significance in both immune function and olfactory-mediated mate choice, the major histocompatibility complex (MHC/MH) is an ideal system in which to evaluate the relative contributions of these two selective forces to genetic diversity. Intrasexual competition and mate choice are both reversed in sex-role reversed species, and sex-related differences in the detection and use of MH-odor cues are expected to influence the intensity of sexual selection in such species. The seahorse, Hippocampus abdominalis, has an exceptionally highly developed form of male parental care, with female-female competition and male mate choice.

Results: Here, we demonstrate that the sex-role reversed seahorse has a single MH class II beta-chain gene and that the diversity of the seahorse MHIIβ locus and its pattern of variation are comparable to those detected in species with conventional sex roles. Despite the presence of only a single gene copy, intralocus MHIIβ allelic diversity in this species exceeds that observed in species with multiple copies of this locus. The MHIIβ locus of the seahorse exhibits a novel expression domain in the male brood pouch.

Conclusions: The high variation found at the seahorse MHIIβ gene indicates that sex-role reversed species are capable of maintaining the high MHC diversity typical in most vertebrates.Whether such species have evolved the capacity to use MH-odor cues during mate choice is presently being investigated using mate choice experiments. If this possibility can be rejected, such systems would offer an exceptional opportunity to study the effects of natural selection in isolation, providing powerful comparative models for understanding the relative importance of selective factors in shaping patterns of genetic variation.

Show MeSH