Literature DB >> 15070747

The ecological and evolutionary consequences of sperm chemoattraction.

Jeffrey A Riffell1, Patrick J Krug, Richard K Zimmer.   

Abstract

Chemical communication between sperm and egg is a critical factor mediating sexual reproduction. Sperm attractants may be significant evolutionarily for maintaining species barriers, and important ecologically for increasing gamete encounters. Still unresolved, however, are the functional consequences of these dissolved signal molecules. Here, we provide experimental evidence that sperm chemoattraction directly affects the magnitude of fertilization success. The recent discovery of L-tryptophan as a potent attractant to red abalone (Haliotis rufescens) sperm affords the opportunity to quantify how navigation affects gamete interactions. Sperm behavioral responses to manipulations of the natural tryptophan gradient around individual eggs reveals that both chemotaxis and chemokinesis significantly promote contacts. Our results show further that attractant release by means of diffusion effectively doubles the target size of red abalone eggs, which in turn significantly increases fertilization success. Although long theorized as potential barriers to hybridization, species-specific sperm attractants in red and green (Haliotis fulgens) abalone are only minor contributors to maintaining reproductive isolation. Because abalone typically live in dense, multispecies aggregations, chemically mediated navigation would prevent sperm from pointlessly tracking heterospecific eggs. Thus, even though reproductive isolation fundamentally resides at the level of membrane recognition proteins, species-specific sperm attractants may evolve to locate the right target within mixed gamete suspensions of closely related species.

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Year:  2004        PMID: 15070747      PMCID: PMC384776          DOI: 10.1073/pnas.0304594101

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  17 in total

1.  Identification of a testicular odorant receptor mediating human sperm chemotaxis.

Authors:  Marc Spehr; Gunter Gisselmann; Alexandra Poplawski; Jeffrey A Riffell; Christian H Wetzel; Richard K Zimmer; Hanns Hatt
Journal:  Science       Date:  2003-03-28       Impact factor: 47.728

Review 2.  The relationship between amino acid sequences of sperm-activating peptides and the taxonomy of echinoids.

Authors:  N Suzuki; K Yoshino
Journal:  Comp Biochem Physiol B       Date:  1992-08

3.  The importance of sperm limitation to the evolution of egg size in marine invertebrates.

Authors:  D R Levitan
Journal:  Am Nat       Date:  1993-04       Impact factor: 3.926

4.  Concerted evolution in an egg receptor for a rapidly evolving abalone sperm protein.

Authors:  W J Swanson; V D Vacquier
Journal:  Science       Date:  1998-07-31       Impact factor: 47.728

5.  A chemoattractant for ascidian spermatozoa is a sulfated steroid.

Authors:  Manabu Yoshida; Michio Murata; Kazuo Inaba; Masaaki Morisawa
Journal:  Proc Natl Acad Sci U S A       Date:  2002-10-31       Impact factor: 11.205

6.  Strong reproductive isolation between closely related tropical sea urchins (genus Echinometra).

Authors:  S R Palumbi; E C Metz
Journal:  Mol Biol Evol       Date:  1991-03       Impact factor: 16.240

7.  Reaction of indole and analogues with amino acid complexes of Escherichia coli tryptophan indole-lyase: detection of a new reaction intermediate by rapid-scanning stopped-flow spectrophotometry.

Authors:  R S Phillips
Journal:  Biochemistry       Date:  1991-06-18       Impact factor: 3.162

8.  An N-terminal partial sequence of the 13 kDa Pycnopodia helianthoides sperm chemoattractant 'startrak' possesses sperm-attracting activity.

Authors:  R L Miller; R Vogt
Journal:  J Exp Biol       Date:  1996-02       Impact factor: 3.312

9.  Nonsynonymous substitution in abalone sperm fertilization genes exceeds substitution in introns and mitochondrial DNA.

Authors:  E C Metz; R Robles-Sikisaka; V D Vacquier
Journal:  Proc Natl Acad Sci U S A       Date:  1998-09-01       Impact factor: 11.205

10.  Fertilization ecology of egg coats: physical versus chemical contributions to fertilization success of free-spawned eggs.

Authors:  Robert D Podolsky
Journal:  J Exp Biol       Date:  2002-06       Impact factor: 3.312

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  15 in total

1.  Gamete plasticity in a broadcast spawning marine invertebrate.

Authors:  Angela J Crean; Dustin J Marshall
Journal:  Proc Natl Acad Sci U S A       Date:  2008-08-29       Impact factor: 11.205

2.  Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria.

Authors:  S A Amin; L R Hmelo; H M van Tol; B P Durham; L T Carlson; K R Heal; R L Morales; C T Berthiaume; M S Parker; B Djunaedi; A E Ingalls; M R Parsek; M A Moran; E V Armbrust
Journal:  Nature       Date:  2015-05-27       Impact factor: 49.962

3.  Chemically moderated gamete preferences predict offspring fitness in a broadcast spawning invertebrate.

Authors:  Mathew Oliver; Jonathan P Evans
Journal:  Proc Biol Sci       Date:  2014-04-16       Impact factor: 5.349

Review 4.  Sexual selection in hermaphrodites, sperm and broadcast spawners, plants and fungi.

Authors:  Madeleine Beekman; Bart Nieuwenhuis; Daniel Ortiz-Barrientos; Jonathan P Evans
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2016-10-19       Impact factor: 6.237

5.  Assessing the potential for egg chemoattractants to mediate sexual selection in a broadcast spawning marine invertebrate.

Authors:  Jonathan P Evans; Francisco Garcia-Gonzalez; Maria Almbro; Oscar Robinson; John L Fitzpatrick
Journal:  Proc Biol Sci       Date:  2012-03-21       Impact factor: 5.349

Review 6.  The role of female reproductive fluid in sperm competition.

Authors:  Clelia Gasparini; Andrea Pilastro; Jonathan P Evans
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2020-10-19       Impact factor: 6.237

Review 7.  Marine chemical ecology: chemical signals and cues structure marine populations, communities, and ecosystems.

Authors:  Mark E Hay
Journal:  Ann Rev Mar Sci       Date:  2009

8.  Sperm chemotaxis, fluid shear, and the evolution of sexual reproduction.

Authors:  Richard K Zimmer; Jeffrey A Riffell
Journal:  Proc Natl Acad Sci U S A       Date:  2011-07-25       Impact factor: 11.205

9.  Mass spectrometry and next-generation sequencing reveal an abundant and rapidly evolving abalone sperm protein.

Authors:  Melody R Palmer; Margo H McDowall; Lia Stewart; Aleena Ouaddi; Michael J MacCoss; Willie J Swanson
Journal:  Mol Reprod Dev       Date:  2013-05-01       Impact factor: 2.609

10.  Lectin staining and flow cytometry reveals female-induced sperm acrosome reaction and surface carbohydrate reorganization.

Authors:  Jukka Kekäläinen; Irma Larma; Matthew Linden; Jonathan P Evans
Journal:  Sci Rep       Date:  2015-10-16       Impact factor: 4.379

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