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

Abstract

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 spermegg 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 five 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 jellycoat 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. The theory of sexual selection holds that, when sperm and males compete, female offspring production should not be limited by sperm availability and females should not be selected for increased mating success (see, e.g., Bateman 1948; Arnold 1994). However, in plants (Burd 1994) and broadcastspawning marine invertebrates (Levitan 1995) pollen and sperm can be limiting, and females in these taxa may also be under selection for increased fertilization success (Burd 1994;Levitan 1996aLevitan , 1998a. This notion has been illustrated in sea urchins, where egg traits appear to be under such selection (Levitan 1993(Levitan , 1996a(Levitan ,b, 1998b. Laboratory and field studies have documented that the percentage of eggs fertilized is correlated with egg size within (Levitan 1996a) and among (Levitan 1993(Levitan , 1998b closely related sea-urchin species and that egg traits may be adapted to particular spawning conditions in ways that optimize fertilization success (Levitan 1993(Levitan , 1996a(Levitan ,b, 1998b Thomas 1994a,b;Podolsky 1995;Podolsky and Strathmann 1996;Styan 1998).What has remained unclear is what attribute of the egg or which component of egg size is actually responsible for increases in fertilization efficiency and what role the jelly coat plays in this interaction (Lillie 1915;Tyler 1941;Hagstrom 1956;Hagstrom and Markman 1957;Levitan 1995;Podolsky 1995;Podolsky and Strathmann 1996;Farley and Levitan 2001). The two factors that determine the fertilization rate of eggs are the rate at which sperm and eggs collide (collision rate) and the rate at which these collisions result in fertilization (fertility rate). The concentration of gametes, ...

Eggs with larger accessory structures are more likely to be fertilized in both low and high sperm concentrations in Styela plicata (Ascidiaceae)

“…In similar experimental designs to the present study, both Podolsky (2001) and Levitan and Irvine (2001) showed that an increase in the jelly coat area of echinoderm eggs is selected for in sperm-limiting conditions. However, Podolsky (2001) argued that as selection pressures were similar for both the ovicell and jelly coat, and jelly coats are cheaper to produce, selection should favour increased investment in jelly coats.…”

“…However, Podolsky (2001) argued that as selection pressures were similar for both the ovicell and jelly coat, and jelly coats are cheaper to produce, selection should favour increased investment in jelly coats. In contrast, Levitan and Irvine (2001) argued that because the unstandardized selection gradient was much steeper for the ovicell, selection should favour increased investment in the ovicell. In our study, we found no selection for ovicell size in sperm-limiting conditions, but instead found that more eggs with smaller ovicells were successfully fertilized in high sperm concentrations.…”

Fertilization Strategies

“…Subsequent studies supported the assertion that physical size of the egg cell influenced fertilization success (e.g. Levitan and Irvine 2001) , whereas others-sometimes working on the very same species-argued for an equally important role of egg accessory structures such as egg jelly or follicle cells (e.g. Podolsky 2001) .…”

“…Rothschild and Swann (1951) , Vogel et al (1982) , Destombe et al (1990), Levitan et al (1991) , Levitan (1993Levitan ( , 2000 , Manríquez et al (2001) , Powell et al (2001), Kupriyanova and Havenhand (2002) , Johnson and Yund (2004) , Levitan et al (2004) , Hodgson et al (2007), Muhlin et al (2008 Size Podolsky (2004) Egg Accessory structures (jelly coat, follicle cells, etc.) Lambert and Lambert (1981), Buckland-Nicks (1993), Farley andLevitan (2001), Levitan and Irvine (2001) , Podolsky (2001Podolsky ( , 2002Podolsky ( , 2004 , Villa and Patricolo (2001) Chemotaxis, chemokinesis Miller (1975Miller ( , 1985 , Maier and Müller (1986 , review), Bolton and Havenhand (1996) , Serrão et al (1996a...…”

Effect of steady and unsteady flow on chemoattractant plume formation and sperm taxis

“…Additionally, the preference of a sperm for certain eggs within a single species (Evans et al, 2012), and viability of both the egg and sperm (Giorgi and DeMartini, 1977) can decrease actual and predicted fertilization rates. In the absence of flow, the effective target size of the egg increases fertilization rates and decreases the negative impact of sperm limitation and sperm dilution (Farley, 2002;Farley and Levitan, 2001;Jantzen et al, 2001;Levitan, 1993Levitan, , 1996Levitan, , 2000Levitan, , 2006Levitan and Irvine, 2001;Styan, 1998).…”