Positive selection and the molecular evolution of a gene of male reproduction, Acp26Aa of Drosophila

Tsaur, Shun-Chern; Wu, Chung‐I

doi:10.1093/oxfordjournals.molbev.a025791

Cited by 209 publications

(125 citation statements)

References 25 publications

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“…For example, in the closely related Hawaiian sea urchins E. oblonga and E. mathaei, alleles at most nuclear loci share clades across species, but bindin is reciprocally monophyletic (Figure 2). Similarly, so-called speciation genes in Drosophila show reciprocal monophyly whereas other genes do not, and show higher rates of amino-acid evolution than other loci (Tsaur and Wu, 1997;Ting et al, 2000). Monophyly produced by more rapid gene coalescence of gamete recognition loci is consistent with directional selection within species, though other evolutionary mechanisms may also generate this pattern (see below).…”

Section: Process and Patterns Of Evolution At Gamete Recognition Locimentioning

confidence: 97%

Speciation and the evolution of gamete recognition genes: pattern and process

2008

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Proteins on gamete surfaces are major determinants of fertilization success, particularly in free-spawning animals. Molecular analyses of these simple genetic systems show rapid evolution, positive selection, accelerated coalescence and, sometimes, extensive polymorphism. Careful analysis of the behavior of sperm produced by males with different gamete alleles shows that these alleles can deliver significant functional differences. Three forms of allele-specific fertilization advantage have been shown: assortative mating based on gamete type, rare allele advantage and heterozygote superiority. Models suggest that sperm and egg proteins may be coevolutionary partners that can alternate between directional selection for high fertilization ability and cyclic adaptation of eggs and sperm driven by sexual conflict. These processes act within allopatric populations and may accelerate their divergence if gamete adaptations in separate demes reduce cross-fertilization. Reproductive character displacement by reinforcement may play a diversifying role when previously allopatric populations rejoin. In circumstance that might prove to be common, divergence in sympatry can be driven by sexual conflict or by association of mating types with ecological differences. The ecology of fertilization, especially the degree of sperm competition and egg death via polyspermy, are important determinants of the strength and direction of selection on gametes. Freespawning animals allow careful analysis of gamete recognition -from the behavior of adults and interactions of gametes, to molecular patterns of allele divergence. Future research efforts on the evolutionary consequences of fertilization ecology, and the interaction between extensive variation in egg surface proteins and sperm fertilization ability, are particularly needed.

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Section: Process and Patterns Of Evolution At Gamete Recognition Locimentioning

confidence: 97%

Speciation and the evolution of gamete recognition genes: pattern and process

2008

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“…mbg.cornell.edu͞wolfner͞tables͞AcpCModels.htm). As a group, Acps are roughly 2-fold more divergent than proteins in nonreproductive tissues (1,9); indeed one, Acp26Aa, is one of the most rapidly evolving genes in the D. melanogaster genome (10,11). This rapid divergence has been suggested to result from positive Darwinian selection (12,13) and to be due to the participation of seminal fluid proteins in the evolutionary dynamics of antagonistic evolution (14), sperm competition (15), and͞or sexual selection (16).…”

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confidence: 99%

“…Reproductive proteins, such as Acps, serve as good candidates for a CM approach, because their rapid evolution generates high levels of sequence diversity (20) yet their structures are likely to remain conserved (21). Here, we used CM to investigate whether there are essential molecular processes in the seminal fluid that are conserved between mammals and flies, despite the differences in reproductive strategies and the fact that many specific Drosophila and mammalian seminal fluid proteins are rapidly evolving (1,(11)(12)(13)(22)(23)(24)(25). Our data illustrate how CM can provide insight into possible functional relationships undetectable by primary sequence alignments.…”

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confidence: 99%

Comparative structural modeling and inference of conserved protein classes in Drosophila seminal fluid

Mueller

Ripoll

Aquadro

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

121

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The constituents of seminal fluid are a complex mixture of proteins and other molecules, most of whose functions have yet to be determined and many of which are rapidly evolving. As a step in elucidating the roles of these proteins and exposing potential functional similarities hidden by their rapid evolution, we performed comparative structural modeling on 28 of 52 predicted seminal proteins produced in the Drosophila melanogaster male accessory gland. Each model was characterized by defining residues likely to be important for structure and function. Comparisons of known protein structures with predicted accessory gland proteins (Acps) revealed similarities undetectable by primary sequence alignments. The structures predict that Acps fall into several categories: regulators of proteolysis, lipid modifiers, immunity͞ protection, sperm-binding proteins, and peptide hormones. The comparative structural modeling approach indicates that major functional classes of mammalian and Drosophila seminal fluid proteins are conserved, despite differences in reproductive strategies. This is particularly striking in the face of the rapid protein sequence evolution that characterizes many reproductive proteins, including Drosophila and mammalian seminal proteins.

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“…O ne of the striking features that has emerged from the study of reproduction is diversity (1)(2)(3)(4)(5)(6)(7)(8)(9)(10)(11)(12)(13)(14)(15)(16)(17). Diversity has been observed in several morphological traits that are involved in reproduction, including sperm (14) and reproductive organ (15) morphology.…”

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confidence: 99%

“…Diversity has been observed in several morphological traits that are involved in reproduction, including sperm (14) and reproductive organ (15) morphology. Recently, male-derived molecules involved in reproduction have been shown to be extraordinarily divergent between closely related species (1)(2)(3)(4)(5)(6)(7)(8)(9)(10)(11)(12)(13). These molecules include proteins involved in signaling between males and females (3)(4)(5), fertilization (6)(7)(8)(9)(10)(11), sperm chromosome condensation (1,12), and sex-specific transcription (16,17).…”

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Positive Darwinian selection drives the evolution of several female reproductive proteins in mammals

Swanson

Yang

Wolfner

et al. 2001

Proc. Natl. Acad. Sci. U.S.A.

422

207

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Rapid evolution driven by positive Darwinian selection is a recurrent theme in male reproductive protein evolution. In contrast, positive selection has never been demonstrated for female reproductive proteins. Here, we perform phylogeny-based tests on three female mammalian fertilization proteins and demonstrate positive selection promoting their divergence. Two of these female fertilization proteins, the zona pellucida glycoproteins ZP2 and ZP3, are part of the mammalian egg coat. Several sites identified in ZP3 as likely to be under positive selection are located in a region previously demonstrated to be involved in species-specific spermegg interaction, suggesting the selective pressure is related to male-female interaction. The results provide long-sought evidence for two evolutionary hypotheses: sperm competition and sexual conflict.zona pellucida ͉ ZP3 ͉ fertilization ͉ sperm competition ͉ sexual conflict

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Positive selection and the molecular evolution of a gene of male reproduction, Acp26Aa of Drosophila

Cited by 209 publications

References 25 publications

Speciation and the evolution of gamete recognition genes: pattern and process

Speciation and the evolution of gamete recognition genes: pattern and process

Comparative structural modeling and inference of conserved protein classes in Drosophila seminal fluid

Positive Darwinian selection drives the evolution of several female reproductive proteins in mammals

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