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Fertilization Selection on Egg and Jelly-Coat Size in the Sand Dollar Dendraster Excentricus

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Fertilization Selection on Egg and Jelly-Coat Size in the Sand Dollar Dendraster Excentricus Evolution, 55(12), 2001, pp. 2479±2483 FERTILIZATION SELECTION ON EGG AND JELLY-COAT SIZE IN THE SAND DOLLAR DENDRASTER EXCENTRICUS DON R. LEVITAN1,2 AND STACEY D. IRVINE2 1Department of Biological Science, Florida State University, Tallahassee, Florida 32306-1100 2Bam®eld Marine Station, Bam®eld, British Columbia VOR 1B0, Canada Abstract. Organisms with external fertilization are often sperm limited, and in echinoids, larger eggs have a higher probability of fertilization than smaller eggs. This difference is thought to be a result of the more frequent sperm- egg collisions experienced by larger targets. Here we report how two components of egg target size, the egg cell and jelly coat, contributed to fertilization success in a selection experiment. We used a cross-sectional analysis of correlated characters to estimate the selection gradients on egg and jelly-coat size in ®ve replicate male pairs of the sand dollar Dendraster excentricus. Results indicated that eggs with larger cells and jelly coats were preferentially fertilized under sperm limitation in the laboratory. The selection gradients were an average of 922% steeper for egg than for jelly- coat size. The standardized selection gradients for egg and jelly-coat size were similar. Our results suggest that fertilization selection can act on both egg-cell and jelly-coat size but that an increase in egg-cell volume is much more likely to increase fertilization success than an equal change in jelly-coat volume. The strengths of the selection gradients were inversely related to the correlation of egg traits across replicate egg clutches. This result suggests the importance of replication in studies of selection of correlated characters. Key words. Correlated characters, echinoids, egg size, fertilization, jelly coat, selection gradient. Received February 15, 2001. Accepted August 26, 2001. The theory of sexual selection holds that, when sperm and The sand dollar Dendraster excentricus (an irregular echi- males compete, female offspring production should not be noid) has a thick jelly coat that increases the egg target di- limited by sperm availability and females should not be se- ameter approximately twofold and the cross-sectional area lected for increased mating success (see, e.g., Bateman 1948; fourfold (Podolsky 1995). We conducted a selection exper- Arnold 1994). However, in plants (Burd 1994) and broadcast- iment by exposing eggs to conditions of sperm limitation and spawning marine invertebrates (Levitan 1995) pollen and examining how egg-cell and jelly-coat size contribute to the sperm can be limiting, and females in these taxa may also likelihood of fertilization. The results suggest that eggs with be under selection for increased fertilization success (Burd large cell size and thick jelly coats are preferentially fertilized 1994; Levitan 1996a, 1998a,b). This notion has been illus- under these conditions but that fertilization selection acts to trated in sea urchins, where egg traits appear to be under such increase the ratio of egg-cell to jelly-coat material. selection (Levitan 1993, 1996a,b, 1998b). Laboratory and ®eld studies have documented that the percentage of eggs MATERIALS AND METHODS fertilized is correlated with egg size within (Levitan 1996a) and among (Levitan 1993, 1998b) closely related sea-urchin We collected D. excentricus from Brady's beach, located species and that egg traits may be adapted to particular in Barkley Sound, British Columbia, Canada (488509N, spawning conditions in ways that optimize fertilization suc- 1258099W), on 8 July 1998. Laboratory experiments were cess (Levitan 1993, 1996a,b, 1998b; Thomas 1994a,b; Po- conducted in July 1998 at the Bam®eld Marine Station, Bam- dolsky 1995; Podolsky and Strathmann 1996; Styan 1998). ®eld, British Columbia. What has remained unclear is what attribute of the egg or We injected sand dollars with 0.55 M KCl to induce spawn- which component of egg size is actually responsible for in- ing. The eggs were collected in ambient-temperature (128C) creases in fertilization ef®ciency and what role the jelly coat ®ltered seawater. The sperm was kept in its dry, concentrated plays in this interaction (Lillie 1915; Tyler 1941; Hagstrom form and placed over ice. 1956; Hagstrom and Markman 1957; Levitan 1995; Podolsky The egg concentration of the stock suspension was adjusted 1995; Podolsky and Strathmann 1996; Farley and Levitan to range from 3000 to 5000 eggs per milliliter. Each of seven 2001). The two factors that determine the fertilization rate scintillation vials was ®lled with 8.0 mL ®ltered seawater of eggs are the rate at which sperm and eggs collide (collision and 1.0 mL of the egg suspension. One of the seven was used rate) and the rate at which these collisions result in fertil- as the control vial and was not fertilized. ization (fertility rate). The concentration of gametes, the A separate series of scintillation vials was used for serially movement of sperm, and the size of the egg target determine diluting sperm. One scintillation vial was ®lled with 9.9 mL the collision rate (Vogel et al. 1982). The fertility rate is a of ®ltered seawater and 0.1 mL of the collected sperm. The more complicated function of the interaction of sperm and sperm suspension was then run through a 10-fold serial di- eggs and is a function of how likely a spermatozoon is to lution into ®ve additional vials, each containing 9.0 mL ®l- penetrate extracellular layers and fuse with the egg cell sur- tered seawater. To each egg vial, 1.0 mL of one of the sperm face. The jelly coat may play a role in both rates, because it suspension was added, such that the six egg vials contained increases the overall target size of the egg and provides a serially diluted sperm. barrier that must be penetrated by the sperm before fertil- Two hours after the addition of sperm, we determined ization is possible. which of the vials produced the fertilization rate closest to 2479 q 2001 The Society for the Study of Evolution. All rights reserved. 2480 D. R. LEVITAN AND S. D. IRVINE 50%. The vial selected always ranged between 45% and 55% The selection differentials (s) for egg and jelly coat volume of eggs fertilized. Unfertilized eggs in that vial (50% fertil- can be calculated as the change in mean size after selection ized) and the control vial (0% fertilized) were measured. (xÅf 2 xÅb). The selection gradient (b) is calculated as Fertilized eggs were not measured because they change shape b5PS21 and size through development (Levitan 1996a). We mixed eggs from both treatments with Sumi ink to vi- where P is the variance-covariance matrix of the characters sualize the jelly coat (Schroeder 1980). Egg-cell and egg-cell- before selection and S is the vector of the selection differ- plus-jelly-coat diameters were measured in 250 eggs per treat- entials (Lande and Arnold 1983). ment and replicate at 1003 under a compound microscope Each replicate was analyzed separately, and paired t-tests with an ocular micrometer. The egg-cell volume and total were conducted to determine whether the selection gradients volume were calculated from these diameter measurements were different from zero and different from one another. The according to the formula for the volume of a sphere. Jelly- selection gradients were also examined as a function of the coat volume was calculated by subtraction of the egg-cell vol- degree of correlation between the traits in each replicate egg ume from the total volume. To ensure that eggs from the clutch. control vials and experimental vials were measured as nearly In our analysis, we choose to use volume as our variable simultaneously as possible, samples of 25±50 eggs from the rather than diameter, cross-sectional area, or a conversion to two sets were measured alternately until all 500 eggs were caloric content. The rationale was that volume is a scale- measured. Each replicate used a different male and female; independent measure of size, whereas a change in diameter ®ve independent replicates of the experiment were conducted. or cross-sectional area in a small egg is hard to compare in the same unit change in a large egg. A conversion to caloric Analysis of Selection on Correlated Characters value was not used because volume and caloric value are poorly correlated within echinoderm species (McEdward and We analyzed data by ®rst conducting paired t-tests of treat- Morgan 2001), rendering an analysis of correlated characters ment and control egg-cell and jelly-coat sizes of unfertilized invalid. Considering caloric investment would be appropriate eggs. We then calculated the selection differentials and gra- in an analysis that included both fertilization and develop- dients (sensu Lande and Arnold 1983) for these correlated ment because energy content may in¯uence postzygotic characters. Because we could not follow the fates of indi- growth and survival. Such an analysis of egg and jelly, using vidual eggs and thus determine the original sizes of the eggs an optimality approach, has been done (Farley and Levitan after fertilization (Levitan 1996a), we compared the two treat- 2001), but for an investigation of fertilization selection, it is ments in a cross-sectional analysis of selection on correlated target size rather than energy content that in¯uences sperm- characters (Lande and Arnold 1983). The cross-sectional egg collisions. method is used when two populations are examined, one before and the other after a round of selection, and is useful RESULTS when paired measurements cannot be made on each individ- ual (in this case eggs). The method can be used if the fol- Mean egg-cell volume ranged from 0.00112 to 0.00135 lowing assumptions can be made: (1) no genetic evolution mm3 and differed signi®cantly across the ®ve females (AN- of the characters has taken place between the two populations; OVA P , 0.0001).
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