Sperm and speciation

Howard, Daniel J.; Palumbi, Stephen R.; Birge, Leanna M.; Manier, Mollie K.

doi:10.1016/b978-0-12-372568-4.00009-4

Cited by 88 publications

(141 citation statements)

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“…Although we have not performed the critical test of this prediction using Female Fertilization Bias 559 within-species variation in male quality, we have demonstrated precisely this mechanism of sperm choice using an extreme case of differential male quality: species identity. When D. simulans females were inseminated by both a D. simulans and a D. mauritiana male, females significantly switched between using sperm predominantly from the SR when the conspecific male mated first and from the spermathecae when the conspecific male mated second, thus biasing fertilization toward conspecific sperm (i.e., conspecific sperm precedence; Price 1997;Howard et al 2009) irrespective of mating order (Manier et al 2013b). Although this may seem unexpectedly sophisticated, biased use of sperm from different storage sites has also been demonstrated for the giant cuttlefish Sepia apama (Naud et al 2005), and there is evidence that females of the damselfly Calopteryx splendens xanthostoma similarly shift between different storage locations differing in composition of competing sperm dependent on the context of oviposition (Siva-Jothy andHooper 1995, 1996).…”

Section: Discussionmentioning

confidence: 99%

“…Female sperm-storage organs enhance sperm survival and temporally separate insemination from fertilization, expanding the temporal, morphological, and biochemical arenas of postcopulatory sexual selection in general, and are predicted to extend the opportunity for female sperm choice in particular (Birkhead et al 1993;Eberhard 1996;Pitnick et al 2009). Sperm-storage organ morphology can be highly diverse (e.g., birds: Birkhead and Møller 1992; pulmonate snails : Baur 1998;spiders: Uhl 2002;insects: Theodor 1976;Puniamoorthy et al 2010;Higginson et al 2012b), rapidly divergent (e.g., Pitnick et al 1999Pitnick et al , 2003 and have been found to exhibit correlated evolution with sperm morphology in diverse taxa (reviewed by Pitnick et al 2009;Higginson et al 2012b), which in turn may promote reproductive isolation between species (Howard et al 2009;Manier et al 2013a). Relatively little is known, however, about female sperm-storage organ function (Schnakenberg et al 2012), particularly with regard to sperm choice.…”

Section: Introductionmentioning

confidence: 99%

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An Analytical Framework for Estimating Fertilization Bias and the Fertilization Set from Multiple Sperm-Storage Organs

Manier

Lüpold

Pitnick

et al. 2013

The American Naturalist

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How sperm from competing males are used to fertilize eggs is poorly understood yet has important implications for postcopulatory sexual selection. Sperm may be used in direct proportion to their numerical representation within the fertilization set or with a bias toward one male over another. Previous theoretical treatments have assumed a single sperm-storage organ, but many taxa possess multiple organs or store sperm within multiple regions of the reproductive tract. In Drosophila, females store sperm in two distinct storage organ types: the seminal receptacle (SR) and the paired spermathecae. Here, we expand previous "raffle" models to describe "fertilization bias" independently for sperm within the SR and the spermathecae and estimate the fertilization set based on the relative contribution of sperm from the different sperm-storage organ types. We apply this model to three closely related species to reveal rapid divergence in the fertilization set and the potential for female sperm choice. Submitted January 18, 2013; Accepted May 15, 2013; Electronically published July 25, 2013 Dryad data: http://dx.doi.org/10.5061/dryad.jd87f.abstract: How sperm from competing males are used to fertilize eggs is poorly understood yet has important implications for postcopulatory sexual selection. Sperm may be used in direct proportion to their numerical representation within the fertilization set or with a bias toward one male over another. Previous theoretical treatments have assumed a single sperm-storage organ, but many taxa possess multiple organs or store sperm within multiple regions of the reproductive tract. In Drosophila, females store sperm in two distinct storage organ types: the seminal receptacle (SR) and the paired spermathecae. Here, we expand previous "raffle" models to describe "fertilization bias" independently for sperm within the SR and the spermathecae and estimate the fertilization set based on the relative contribution of sperm from the different sperm-storage organ types. We apply this model to three closely related species to reveal rapid divergence in the fertilization set and the potential for female sperm choice.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

An Analytical Framework for Estimating Fertilization Bias and the Fertilization Set from Multiple Sperm-Storage Organs

Manier

Lüpold

Pitnick

et al. 2013

The American Naturalist

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“…Sperm is known to evolve very rapidly [9] and divergence in sperm characteristics between the parental species could lead to suboptimal fertilization capacity in hybrids with intermediate sperm traits. The severity of problems affecting hybrid sperm should depend on the degree of divergence rsbl.royalsocietypublishing.org Biol Lett 9: 20130169 between the parental species.…”

Section: Discussionmentioning

confidence: 99%

“…Furthermore, the sperm of hybrid males may also compete poorly against pure-species sperm, and mechanisms of cryptic female choice may be at play [9]. In addition, hybrid males may produce low quantities of sperm, or the sperm may swim poorly or fail to fuse with eggs because of incompatibilities between reproductive proteins [9].…”

Section: Introductionmentioning

confidence: 99%

Low fertility of wild hybrid male flycatchers despite recent divergence

et al. 2013

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Postzygotic isolation may be important for maintaining species boundaries, particularly when premating barriers are incomplete. Little is known about the course of events leading from minor environmental mismatches affecting hybrid fitness to severe genetic incompatibilities causing sterility or inviability. We investigated whether reduced reproductive success of hybrid males was caused by suboptimal sperm traits or by more severe genetic incompatibilities in a hybrid zone of pied (Ficedula hypoleuca) and collared flycatchers (F. albicollis) on the island of Ö land, Sweden. About 4 per cent hybridization is observed in this population and all female hybrids are sterile. We found no sperm in the ejaculates of most sampled hybrid males, and sperm with abnormal morphology in two hybrids. Furthermore, none of the hybrids sired any offspring because of high levels of hatching failure and extrapair paternity in their nests. These results from a natural hybrid zone suggest that the spermatogenesis of hybrid males may become disrupted despite little genetic divergence between the parental species.

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“…C are fertilized by conspecific sperm at much higher rates (Geyer and Palumbi, 2005). Such conspecific sperm precedence ( Figure 1) is a common feature of internally fertilizing insects and mammals (Howard, 1999;Howard et al, 2008), but has rarely been tested for explicitly among broadcast spawners.…”

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confidence: 99%

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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Sperm and speciation

Cited by 88 publications

References 204 publications

An Analytical Framework for Estimating Fertilization Bias and the Fertilization Set from Multiple Sperm-Storage Organs

An Analytical Framework for Estimating Fertilization Bias and the Fertilization Set from Multiple Sperm-Storage Organs

Low fertility of wild hybrid male flycatchers despite recent divergence

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

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