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Repeatability of Egg Size in Two Marine Gastropods: Brood Order and Female Size Do Not Contribute to Intraspecific Variation

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Repeatability of Egg Size in Two Marine Gastropods: Brood Order and Female Size Do Not Contribute to Intraspecific Variation Vol. 410: 89–96, 2010 MARINE ECOLOGY PROGRESS SERIES Published July 14 doi: 10.3354/meps08638 Mar Ecol Prog Ser Repeatability of egg size in two marine gastropods: brood order and female size do not contribute to intraspecific variation Rachel Collin* Smithsonian Tropical Research Institute, Box 0843-03092, Balboa, Republic of Panama Address for correspondence: Smithsonian Tropical Research Institute, Unit 0948, APO AA 34002, USA ABSTRACT: Egg size has been shown to vary among females in many species of marine inverte- brates and fishes. Usually, however, only a single reproductive event is measured for each female, leaving open the possibility that egg size could vary significantly among broods from the same female. Here I measured egg size from 3 to 7 broods per female from 2 calyptraeid species, Crepidula atrasolea and C. ustulatulina, in 2 experiments. In a preliminary experiment, females were raised from hatching under constant temperature in incubators; in a second larger experiment, they were raised under varying temperatures on the laboratory bench top. Under both conditions, there were significant differences in egg size among broods from each female, as well as significant differences among females from the bench top. Estimates of repeatability, which give an upper boundary on the heritability of a trait, were significantly reduced when among brood variation was included in the cal- culations, suggesting that caution should be used in interpreting among-female components of vari- ation in studies that measure only a single brood per female. Egg size was not related to female size, and there was an effect of brood order on egg size in only C. ustulatulina from the bench top. Eggs produced in the incubators were larger than those from the bench top and they were more variable within broods, resulting in a lower repeatability of egg size from incubator animals than from bench top animals. The significant variation in egg size at all levels of the analysis suggests that such varia- tion should be included in models of egg size evolution, and that the evolutionary dynamics of egg size may be more complicated than reflected in current models of life-history evolution. KEY WORDS: Crepidula · Direct development · Phenotypic plasticity · Bet-hedging Resale or republication not permitted without written consent of the publisher INTRODUCTION upon which they act. Bernardo (1996) pointed out that detailed data documenting intraspecific variation in Egg size is a feature of great importance in the evo- propagule size is simply not available for many organ- lution of life histories and can vary widely among isms, and such data are especially rare for most groups closely related species. Interspecific differences are of marine invertebrates (see reviews by Hadfield & common in many groups of marine invertebrates and Strathmann 1996, Marshall & Keough 2008, Moran & recent molecular phylogenetic evidence has shown McAlister 2009). that a number of these differences have evolved There are few published studies that are explicitly rapidly (Collin 2004, Hart & Podolsky 2005, Collin et al. focused on intraspecific variation in egg size (usually 2007). The evolutionary processes by which these measured as egg diameter) in marine invertebrates, interspecific differences in egg size develop are not but those that are available generally report significant well understood and, like the evolutionary transforma- differences among females. For example, a detailed tion of any feature, the key to such understanding lies study of egg size in 13 species of tropical echinoids dis- in intraspecifc processes and the intraspecific variation covered significant differences in egg size among *Email: [email protected] © Inter-Research 2010 · www.int-res.com 90 Mar Ecol Prog Ser 410: 89–96, 2010 females in each species (Lessios 1988). Phillips (2007) female variation are reported explicitly. In a literature found that 20% of the variation in egg size and 86% of review of patterns in offspring size (measured as hatch- the variation in energy content in mussel eggs were ing size) variability in 25 marine invertebrates, Mar- due to variation among field-collected females. Collin shall et al. (2008) found that the CVs in offspring size & Salazar (2010) found that 65% of the variation in egg among and within females (from a single clutch) ranged size of laboratory raised slipper snails Crepidula atra- from 1.6 to 22.9 and 2.0 to 25.7 respectively, suggesting solea and C. ustulatulina was due to variation among that variation at both levels is common. The small num- females. Reviews of variation in vertebrate egg size ber of invertebrate species for which these values could also commonly find significant variation among fe- be calculated (only 18 were from published studies) males. For example, a review of 26 studies of bird egg and the small sample sizes for many of them are also volume found that an average of 70% of the intraspe- typical of the sparse literature on both invertebrates cific variance could be attributed to variation among and nonavian vertebrates (Christians 2002). females (Christians 2002). Studies demonstrating that The few cases where egg size has been examined >50% of the variance in egg size is due to variation from multiple broods from individual females in ma- among females are also common in fish, reptiles and rine invertebrates generally show a reduction in egg amphibians (reviewed by Christians 2002). size with brood order or over time. A study of the nudi- In all of the invertebrate studies listed above, a single branch Adalaria proxima from several sites around the spawning event was examined from each female, and northern UK found that egg size not only varied among only a few females were measured in many cases. sites, but also decreased with the age of the mother Consequently, while the among female component of (Jones et al. 1996). Likewise, egg size and the number variation in egg size could be calculated, the within of eggs per egg mass decreased with time after the female component could at best be approximated from onset of reproduction in the opisthobranch Haloa the residual variance, and could not be broken down japonica (Ito 1997); egg size decreased with age in the into within and among brood components. If clutches nudibranch Tenellia adspersa (Chester 1996, see his vary through time, seasonally, or with maternal age or Fig. 3); and egg size and egg number decreased with size, the within female component of variation could age in the polychaete Capitella sp. (Qian & Chia 1992). be higher relative to the among female component These are all short-lived weedy or annual species that than is indicated from the results of these studies. generally reproduce for a season and then die. It was Since the relative amounts of within and among female suggested in each study that the observed decreases in variance contributing to phenotypic variation can be egg size were due to reduction in adult size resulting used to calculate the repeatability of a trait, and there- from limited feeding after the onset of reproduction, or fore set an upper boundary on its heritability (Falconer the detrimental effects of aging. Similar decreases in & Mackay 1996), it is important to obtain accurate esti- propagule size with age have been reported for short- mates of these variance components. lived terrestrial species including the housefly (McIn- Data from studies that explicitly examine variation in tyre & Gooding 2000), a parasitic wasp (Giron & Casas egg size within and among broods are not only neces- 2003), some butterflies (Fischer et al. 2003), and 8 sary to calculate repeatability, but are also necessary to weedy herbaceous plants (Cavers & Steel 1984). Egg test some of the newly proposed hypotheses about dif- size has occasionally been reported to increase with ferences in offspring variability between direct devel- age in arthropods (e.g. soil mites, Benton et al. 2005), opers and species with planktotrophic larvae. For but this is less common than a reduction in egg size example, in a review of 102 marine invertebrates, Mar- (reviewed by Fox & Czesak 2000). An exception to this shall & Keough (2008) noted that direct developers that general pattern appears in birds, which often show a produce large propagules showed greater within spe- slight but significant increase in egg size with age or cies variation in offspring size than did species with experience (Christians 2002). planktotrophic development and small propagules. A Previous studies of egg size and hatching size in possible explanation for this pattern was put forward species of Crepidula, a genus of protandrous, filter- by Marshall et al. (2008) who predicted that offspring feeding marine gastropods, have demonstrated signifi- of direct developers should vary less within each cant intraspecific variation in egg size. Measurements female and more among females, than do the offspring of eggs produced in the laboratory showed that egg of planktotrophs. This is because mothers of direct size varies with temperature and can vary among geo- developers should be better able to predict the condi- graphically distinct populations (Collin & Salazar 2010). tions that will be experienced by their offspring that Despite the effects of these factors, more than half of settle nearby, than mothers of planktotrophic larvae. the observed variation in egg size was due to variation There are very few published studies of offspring size among females. This variation did not seem to be due to in marine invertebrates where both among and within female size. Since only a single brood was measured Collin: Egg size in Crepidula 91 per female, it was not possible to examine the details of attached to the substrate and brooded between the the within female variation in egg size, which is the female’s neck and propodium. Within the capsules, the focus of the present study. I measured egg size from eggs are not surrounded by extraembryonic mem- multiple broods from numerous females of the same 2 branes; therefore, the egg measurements reported species, Crepidula atrasolea and C.
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