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Sperm Chemotaxis, Fluid Shear, and the Evolution of Sexual Reproduction

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Sperm Chemotaxis, Fluid Shear, and the Evolution of Sexual Reproduction Sperm chemotaxis, fluid shear, and the evolution of sexual reproduction Richard K. Zimmera,b,1,2 and Jeffrey A. Riffellc,1,2 aDepartment of Ecology and Evolutionary Biology and bNeurosciences Program and Brain Research Institute, University of California, Los Angeles, Los Angeles, CA 90095-1606; and cDepartment of Biology, University of Washington, Seattle, WA 98195 Edited by George N. Somero, Stanford University, Stanford, CA, and approved June 28, 2011 (received for review December 13, 2010) Chemical communication is fundamental to sexual reproduction, concentration gradients (11, 13) and thus promoting chemotaxis. but how sperm search for and find an egg remains enigmatic. For Previous investigations have elucidated specific mechanisms that red abalone (Haliotis rufescens), a large marine snail, the relation- underlie sperm motility (reviewed in refs. 15, 16). They have not, ship between chemical signaling and fluid motion largely deter- however, provided the information necessary for predicting emer- mines fertilization success. Egg-derived attractant plumes are gent properties of sperm–egg interactions as a consequence of dynamic, changing their size and shape in response to unique combined physical, chemical, and biological factors. combinations of physical and chemical environmental features. Soluble sperm attractants could mediate fertilization success Attractant plumes that promote sexual reproduction, however, and drive speciation, operating upstream of cell-surface proteins are limited to a precise set of hydrodynamic conditions. Perfor- and before gamete contact (17–19). Although purportedly critical mance-maximizing shears are those that most closely match flows in sexual reproduction, the influence of gamete chemical com- in native spawning habitats. Under conditions in which reproduc- munication on fertilization in flow has been inferred, but never tive success is chronically limited by sperm availability, gametes tested directly to our knowledge. Recent discoveries have con- are under selection for mechanisms that increase sperm–egg en- siderably improved knowledge on the molecular basis of signal counter. Here, chemoattraction is found to provide a cheap evolu- transduction and sperm chemotaxis (20, 21). Still, we are aware of tionary alternative for enhancing egg target size without enlarg- no experimental evidence demonstrating, unequivocally, a cause- ing cytoplasmic and/or cell volume. Because egg signaling and and-effect relationship among sperm chemoattraction, fluid mo- fi fl sperm response may be tuned to meet speci c uid-dynamic con- tion, and fertilization success. straints, shear could act as a critical selective pressure that drives The identification of a signal molecule links behavioral perfor- fi gamete evolution and determines tness. mance with ecological and evolutionary consequences. Red aba- lone (Haliotis rufescens) sperm detect a waterborne chemical cue invertebrate sperm chemotaxis | mammalian sperm chemotaxis | emitted by conspecific eggs, and change their swimming behavior small-scale turbulence to increase the likelihood of successful contact (22). As determined by bioassay-guided fractionation of natural egg-conditioned sea- hemical communication is pervasive among gametes of taxa water, male gamete attraction is dose-dependent and stereospe- Cwith diverse reproductive strategies. Sperm activation and cific for the L-isomer of tryptophan (23). This same compound fails chemotaxis occur in marine animals and plants that broadcast to elicit behavioral responses from the sperm of three congeneric gametes into the sea, as well as in terrestrial organisms with in- abalone species (Haliotis sorenseni, Haliotis corrugata,orHaliotis ternal fertilization (1–6). At the scale of gamete interactions (0.01– fulgens) that inhabit the same coastal environments and overlap in 1mm;Re<< 1; the Reynolds number is a dimensionless ratio, reproductive timing with H. rufescens. Waterborne compounds, reflecting the magnitude of inertial forces to viscous forces that act upon release from each of the three species, do not affect the fl on a body in ow), sperm encounter eggs while being transported sperm of red abalone. Moreover, L-tryptophan metabolites, in- within a laminar (i.e., viscous) shear flow. The magnitudes of shear cluding serotonin, tyramine, and seven other structural analogues, forces in mammalian reproductive tracts are remarkably similar to do not impact H. rufescens sperm motility or orientation toward those in many coastal ocean environments (7–14). Consequently, eggs (24). Consequently, red abalone sperm require only a single, mechanisms that drive sperm–egg interactions for external-fertil- identified compound for conspecific gamete attraction. izing marine organisms are informative of processes that operate in In this study, we simulated critical aspects of small-scale turbu- their internal-fertilizing terrestrial counterparts. lence within the natural habitats of spawning red abalone (Fig. 1). Experimental studies on sperm behavior traditionally have Laminar-shear was manipulated systematically in large Taylor– been conducted in still water. However, most gametes populate Couette flow tanks (Fig. S1). Sperm motility, gamete encounter a natural world of fluid motion. In the ocean, sperm and eggs rate, and fertilization success all were quantified, simultaneously, by usually are smaller than the tiniest vortices at these viscous- using a custom-built IR laser and computer-assisted digital imaging fl fi dominated scales (11, 12). The microscopic ow elds consist of system. Combining theoretical and empirical approaches, egg-de- — instabilities that give rise to laminar shear (10) the change in rived tryptophan plumes were described accurately and linked to velocity divided by change in distance. Such shears also are gen- sperm locomotory performance. Boundary conditions for 3D nu- erated in a terrestrial, mammalian reproductive tract, in which merical modeling (flow speed, fluid shear, tryptophan release rate flows are driven by muscular contractions, ciliary beating, and/or convective heating (8, 9, 14). Here, laminar shears result from the fl fi viscous ows produced in con ned passages. Whether gametes Author contributions: R.K.Z. and J.A.R. designed research, performed research, analyzed are suspended in a relatively unbounded (e.g., ocean) or bounded data, and wrote the paper. (e.g., vessel) medium, or attached to a surface, the magnitude of The authors declare no conflict of interest. – shear has important consequences for sperm egg interactions. This article is a PNAS Direct Submission. A given shear can positively or negatively affect gamete perfor- 1R.K.Z. and J.A.R. contributed equally to this work. mance. In excessive shears, for example, sperm may lose control of 2To whom correspondence may be addressed. E-mail: [email protected] or jriffell@ their swimming direction, which would impede chemotaxis and in- u.washington.edu. hibit fertilization (12, 13). Alternatively, higher shears could thin the This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. boundary layer in specific regions near a rotating egg, steepening 1073/pnas.1018666108/-/DCSupplemental. 13200–13205 | PNAS | August 9, 2011 | vol. 108 | no. 32 www.pnas.org/cgi/doi/10.1073/pnas.1018666108 Downloaded by guest on October 2, 2021 Fig. 1. (A) Open habitat of giant kelp forest in shallow (10–15 m depth) coastal waters offshore of Point Loma, San Diego, California (photo by Eric Hanauer). (Scale bar, 25 cm.) (B) Within this forest (and others like it), adult red abalone ag- gregate underneath ledges and in crevices among rocky reefs. Hydrodynamic measurements have characterized the physical properties of these environments (13). Relatively strong cross- shelf and weak longshore currents are typical of open reef habitats. In contrast, flow speeds among the rocky ledges and crevices harboring groups of red abalone (”hot spots”) are two to three times slower than in exposed areas. These hot spots exhibit significantly smaller Reynolds stresses, turbulent energy dissipation rates, and shears (ranging from 0.3 to 2.4 s−1 and − from 4.8 to 13.4 s 1 in hot spots and open habitats, re- spectively; ref. 13). Red abalone thus aggregate and spawn at sites where water motion is relatively tranquil. Critical aspects of these flow environments can be simulated within a Taylor– Couette apparatus (photo by Eric Hanauer). (Scale bar, 15 cm.) (C) Each adult male or female spawns gametes into the sea via excurrent tremata, small holes in the shell that connect the mantle cavity (i.e., exit site for reproductive products) and surrounding ocean. The epipodium (i.e., lateral lobe of the foot) contains many small tentacles that are used in sensing water motion; two large cephalic tentacles (not shown) pro- trude from the head (arrow at left) and function primarily in olfaction (photo by Luis Ignacio-Vilchis). (Scale bar, 1.0 cm.) (D) Spawning of sperm by a single adult male. Propulsive forces generated by the muscular contractions of its foot ultimately produce a gamete jet, or plume. In nature, both mature males and females are gravid yearround and spawn synchronously. Individuals can be systematically induced to spawn in the laboratory, and a single gravid male or female releases approximately 10 billion sperm or 3 million eggs, respectively. Profuse gamete material is therefore available at almost all times for laboratory experiments (photo by Larry Friesen and Daniel Morse). (Scale bar, 0.5 cm.) and diffusion coefficient, egg rotational
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