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The rapid evolution of reproductive proteins

Key Points

  • Many genes that are involved in different aspects of sexual reproduction evolve at rapid rates. For example, when rodent and human gene sequences are compared, many reproductive genes are found among the 10% most divergent genes.

  • In some cases, the rapid evolution of reproductive proteins is promoted by adaptive evolution, which indicates that a functional benefit underlies their rapid divergence.

  • The selective pressures that drive the evolution of reproductive proteins could include: sperm competition, cryptic female choice and sexual conflict.

  • The coevolution of corresponding (interacting) female and male pairs of reproductive proteins could be a factor in the establishment of barriers to fertilization, which leads to reproductive isolation between populations and, perhaps, the establishment of new species.

Abstract

Many genes that mediate sexual reproduction, such as those involved in gamete recognition, diverge rapidly, often as a result of adaptive evolution. This widespread phenomenon might have important consequences, such as the establishment of barriers to fertilization that might lead to speciation. Sequence comparisons and functional studies are beginning to show the extent to which the rapid divergence of reproductive proteins is involved in the speciation process.

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Figure 1: Rapidly evolving proteins.
Figure 2: Lysin–VERL coevolution might lead to the evolution of species-specific fertilization.
Figure 3: The main events in the sperm–egg interaction.

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Acknowledgements

V.D.V. is supported by the National Institutes of Health and W.J.S. by the National Science Foundation. C. F. Aquadro, M. F. Wolfner, J. D. Calkins, J. P. Vacquier, M. E. Hellberg and two anonymous reviewers are thanked for their critical reading of the manuscript.

This article will appear as part of a web focus on the evolution of sex, which will coincide with our forthcoming special issue on this topic.

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Correspondence to Willie J. Swanson.

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DATABASES

LocusLink

Acp26Aa

Acp29AB

Acp36DE

ACR

β-fertilin

Ph-20

TCTE1

zonadhesin

ZP1

ZP2

ZP3

FURTHER INFORMATION

Speciation: allopatric

Speciation: sympatric and parapatric

Glossary

ADAPTIVE EVOLUTION

A genetic change that results in increased fitness.

ORTHOLOGOUS GENES

Homologous genes in different species that derive from a common ancestral gene without gene duplication or horizontal transmission.

PURIFYING SELECTION

Selection against a deleterious allele.

MAXIMUM LIKELIHOOD

The maximum-likelihood method takes a model of sequence evolution (essentially a set of parameters that describe the pattern of substitutions) and searches for the combination of parameter values that gives the greatest probability of obtaining the observed sequences.

CILIATE

A single-celled protist with a micronucleus (germ-line nucleus), a macronucleus (somatic nucleus), and cilia for swimming and capturing food.

CONJUGATION

The joining of two cells for the transfer of genetic material.

DIATOM

A unicellular alga that is important in global photosynthesis and carbon cycling.

INBREEDING DEPRESSION

Loss of vigour owing to homozygosity of an increasing number of genes; it occurs as a consequence of mating between closely related individuals.

SPOROPHYTE

In plants that undergo alternation of generations, a multicellular diploid form that results from a union of haploid gametes and that meiotically produces haploid spores, which will in turn grow into the gametophyte generation.

SIGNAL SEQUENCE

A short sequence on a newly translated polypeptide that serves as a signal for its transfer to the correct subcellular location.

GAMETOPHYTE

In a reproductive cycle of a plant, a generation that has a haploid set of chromosomes and produces gametes.

ACROSOME

A secretory organelle in the sperm head.

SYMPATRIC

Having overlapping geographical distributions.

GENE CONVERSION

The non-reciprocal transfer of information between homologous genes as a consequence of heteroduplex formation followed by repair mismatches.

GASTROPOD

A class in the phylum Mollusca that is characterized by a muscular foot, on which the body rests, and a single shell. Examples include snails, limpets, sea hares and abalone.

POLYMORPHISM

Occurrence, at a single genetic locus, of two or more alleles that differ in nucleotide sequence.

ASSORTATIVE MATING

Non-random mating; it occurs when individuals select their mates on the basis of one or more physical or chemical characteristics.

SEXUAL SELECTION

Selection for characteristics that enhance mating success.

QUANTITATIVE TRAIT

A measurable trait that depends on the cumulative action of many genes (or quantitative trait loci).

ALLOPATRIC

Having non-overlapping geographical distributions.

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Swanson, W., Vacquier, V. The rapid evolution of reproductive proteins. Nat Rev Genet 3, 137–144 (2002). https://doi.org/10.1038/nrg733

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