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The Role of Jelly Coats in Sperm-Egg Encounters, Fertilization Success, and Selection on Egg Size in Broadcast Spawners

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The Role of Jelly Coats in Sperm-Egg Encounters, Fertilization Success, and Selection on Egg Size in Broadcast Spawners vol. 157, no. 6 the american naturalist june 2001 The Role of Jelly Coats in Sperm-Egg Encounters, Fertilization Success, and Selection on Egg Size in Broadcast Spawners Gregory S. Farley* and Don R. Levitan† Department of Biological Science, Florida State University, 1996a, 1998b; Coma and Lasker 1997). The proposed mech- Tallahassee, Florida 32306-1100 anism generating this result is simply that larger egg targets are more likely to be struck by swimming sperm (Rothschild Submitted February 2, 2000; Accepted January 19, 2001 and Swann 1949, 1951; Vogel et al. 1982). This finding has generated the hypothesis that sperm availability can influ- ence the evolutionary trade-off between egg size and num- ber (Levitan 1993, 1996a, 1996b, 1998a, 1998b). However, abstract: Sperm limitation may be an important selective force the idea that fertilization kinetics might influence this trade- influencing gamete traits such as egg size. The relatively inexpensive off has been challenged because of the notion that extra- extracellular structures surrounding many marine invertebrate eggs might serve to enhance collision rates without the added cost of cellular structures or chemoattractants may increase sperm- increasing the egg cell. However, despite decades of research, the egg collisions yet may not represent as great a cost to effects of extracellular structures on fertilization have not been con- fecundity as the trade-off associated with increased egg size clusively documented. Here, using the sea urchin Lytechinus varie- (Podolsky and Strathmann 1996; Styan 1998). These con- gatus, we remove jelly coats from eggs, and we quantify sperm col- tradictory ideas have not been resolved because data de- lisions to eggs with jelly coats, eggs without jelly coats, and inert tailing the influence of extracellular materials on fertilization plastic beads. We also quantify fertilization success in both egg treat- success are equivocal and because there have been no studies ment groups. We find that sperm-egg collision rates increase as a function of sperm concentration and target size and that sperm are to date that have empirically quantified collision frequencies not chemotactically attracted to eggs nor to jelly coats in this species. between sperm and eggs. In fertilization assays, the presence of the jelly coat is correlated with The eggs of many echinoderms are surrounded by jelly a significant but smaller-than-expected improvement in fertilization coats that can increase the diameter of the egg package by success. A pair of optimality models predict that, despite the large 100% or more (Harvey 1956). If increasing the overall target difference in the energetic value of egg contents and jelly material, size of the egg package increases sperm-egg collision fre- the presence of the jelly coat does not diminish selection for larger quency, as predicted by theoretical models of fertilization egg cell size when sperm are limiting. kinetics (Rothschild and Swann 1949, 1951; Vogel et al. 1982), then jelly coats might be an efficient mechanism for Keywords: collisions, egg size, jelly coat size, fertilization, selection. enhancing fertilization (Rothschild and Swann 1951; Epel 1991; Podolsky and Strathmann 1996; Styan 1998). Jelly When sperm are limiting, selection can act on both male coats might also affect fertilization by attracting sperm and female traits for enhanced fertilization success (Levitan chemically, eliminating the need for a physical structure to 1993, 1996a, 1996b, 1998a, 2000b; Arnold 1994; Burd 1994). enhance target size. Sperm chemotaxis to egg extracts has Broadcast spawning invertebrates are often sperm limited, been demonstrated in several taxa, including echinoderms, and laboratory and field studies have documented that but numerous assays using echinoid egg extracts have failed larger eggs, within and among species, are preferentially to attract sperm (Miller 1985a, 1985b). The only demon- fertilized under sperm-limited conditions (Levitan 1993, stration of sperm chemotaxis in sea urchins involves the attraction of sperm to a component of the jelly coat in one * E-mail: [email protected]. species (Arbacia punctulata; Ward et al. 1985). No studies † E-mail: [email protected]. to date have demonstrated chemotaxis to whole eggs or Am. Nat. 2001. Vol. 157, pp. 626–636. ᭧ 2001 by The University of Chicago. determined whether chemotaxis results in increased levels 0003-0147/2001/15706-0004$03.00. All rights reserved. of fertilization. Sperm-Egg Collisions 627 Despite half a century of laboratory investigations com- virgin eggs (E0; eggs/mL), the time of sperm-egg exposure 3 paring fertilization in the presence and absence of the jelly (t; s), a rate constant describing collisions (b0;mm/s), and coat (Tyler 1941; Rothschild and Swann 1951; Hagstro¨m a rate constant describing fertilization (b;mm3/s): 1956a, 1956b; Hagstro¨m and Markman 1957; Podolsky Ϫ Ϫ Ϫb Et 1995), the evidence is ambiguous. Most studies suggest that F p 1 Ϫ e ( bS000/b E )(1 e 00).(1) removal of the jelly coat decreases the fraction of eggs fer- tilized at a given sperm concentration (Tyler 1941; Roths- The rate constant describing sperm-egg collisions (b0)is child and Swann 1951; Hagstro¨m 1956b; Podolsky 1995). estimated by multiplying sperm swimming speed (n; mm/ Hagstro¨m (1956b) also demonstrated the opposite result s) and the area of the egg cross section (j;mm2): and suggested that decreases in fertilization success among jelly-free eggs were caused by the extremely acidic washes p b0 nj,(2) that previous investigators had used to remove jelly coats from eggs. In contrast, studies that quantified the rate, rather wherej p p(egg radius)2 . than the final percent, of eggs fertilized suggest that removal Using empirical estimates for the proportion of eggs of the jelly coat causes an increase in fertilization, regardless fertilized in a sample (F), the initial sperm concentration of the method by which jelly coats were removed (Hagstro¨m (S0), the initial egg concentration (E0), the time of sperm- 1956a; Hagstro¨m and Markman 1957). There are two prob- egg exposure (t), and the rate constant describing collisions lems with these studies: first, the possibility that eggs were (b0), the model can be solved to estimate the value of the damaged during jelly coat removal makes the impact of the fertilization rate constant (b) with nonlinear regression jelly coat on fertilization difficult to interpret; and second, (Marquardt method; SAS 1996). Once these parameters these fertilization assays do not provide direct evidence of have been estimated, the formula can be solved for the the frequencies of sperm-egg collisions. concentration of sperm needed to fertilize 50% of eggs. Here, by directly observing gametes of the sea urchin This provides an intuitive measure of gamete performance. Lytechinus variegatus, we quantify the number of collisions The ratiob/b0 is another useful measure that provides an between sperm and eggs. By comparing collision frequency indication of fertilization efficiency. This ratio of the es- among eggs with intact jelly coats, eggs gently stripped of timated fertilization constant to the collision constant has jelly coats, and inert plastic beads, we explore the impor- three possible interpretations: the proportion of colliding tance of target size to sperm-egg collision frequency, and sperm that initiate fertilization, the fraction of the egg we test for chemotactic attraction of sperm to egg jelly or surface available for fertilization (Vogel et al. 1982), or the to eggs. To explore the impact of jelly coat removal on the proportion of sperm that is viable. proportion of eggs fertilized, we remove jelly coats using Styan (1998) modified the VCCW model to account for only seawater and assay fertilization. Using a fertilization zygote loss due to polyspermy. Polyspermy is a develop- kinetics model developed by Styan (1998), we compare the mental failure caused by multiple sperm penetrating the egg predicted effect of removing jelly coats on fertilization with and has been noted in nature (Brawley 1992) and in the empirical measures of fertilization. Finally, to estimate how laboratory (Styan and Butler 2000) when eggs are exposed selection might influence both egg provisioning and the to high sperm concentrations. Styan’s (1998) model sub- thickness of the jelly coat, we present a model that predicts tracts away polyspermic zygotes from all zygotes to predict the optimal egg and jelly coat size as a function of sperm the proportion of monospermic zygotes (Jmono) as follows: limitation. J p 1 Ϫ eϪx Ϫ (1 Ϫ eϪx Ϫ xeϪx)(1 Ϫ eϪb), (3) Material and Methods mono Models of Fertilization Kinetics with Perhaps the most widely used model of fertilization kinetics bS0 Ϫ was developed by Vogel et al. (1982; their “Don Ottavio” x p ()1 Ϫ e b00Et,(4) model, hereafter “VCCW”). The model was derived from b00E principles of molecular kinetics, so it assumes Brownian motion of eggs and sperm. It also assumes permanent ad- and hesion of a sperm to the first egg with which it collides. bS0 Ϫ In the VCCW model, the proportion of eggs fertilized in b p ()1 Ϫ e b00bEt .(5) a sample (F) is predicted as a function of the initial sperm b00E concentration (S0; sperm/mL), the initial concentration of 628 The American Naturalist The new variable tb is the time (s) necessary to establish (on the order noted in crashing waves) to damage gametes a block to polyspermy. to the point where subsequent fertilization is affected Empirical data confirm that variation in gamete traits (Mead and Denny 1995; Thomas et al. 1999; M. Denny, can influence fertilization. As predicted by these kinetics personal communication). We placed eggs to be stripped models, increases in sperm velocity (Levitan 2000b), gam- into a 250-mL beaker, covered them with approximately ete longevity (Pennington 1985; Havenhand 1991; Oliver 50 mL of fresh artificial seawater, and gently rotated the and Babcock 1992; Benzie and Dixon 1994), sperm-egg beaker by hand at three revolutions per second for 20 min contact time (Levitan et al.
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