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Optimal Egg Size in Marine Invertebrates: Theory and Phylogenetic Analysis of the Critical Relationship between Egg Size and Development Time in Echinoids
Abstract
Life-history models for marine invertebrate larvae generally predict a dichotomy in egg size in different species: eggs should be either minimal in size or large enough to support development fully without larval feeding. This prediction is contradicted, however, by the empirical observation of wide, continuous variation in egg size between these extremes. The prediction of dichotomy rests on the assumption of a negative linear relationship between egg size and development time. Here, I present a simple model in which development time is inversely proportional to egg size. Incorporating this relationship into an optimality model produces predictions of intermediate rather than extreme egg size. Modeled variations in mortality, food availability, fertilization rates, and temperature all produce continuous shifts in the value of the intermediate optimal size, in direct contrast to those produced by previous models, which predict shifts between two extreme optima. Empirical data on echinoid egg size and development time strongly support the model's assumption of an inverse proportional relationship between egg size and development time. A composite phylogeny is constructed of the 37 species for which egg size, development time, water temperature, and phylogenetic relatedness are known. Independent contrasts are made of the evolutionary changes in egg size and development time. This analysis indicates that evolutionary shifts in development time are correlated with the inversely proportional shifts in egg size assumed in the model. The assumption of a negative linear relationship used in previous models is rejected. This model provides a potential explanation for intraspecific variation in egg size along environmental gradients, sympatric differences in egg size among species, and biogeographic trends in egg size and development mode across taxa.
... When mean currents are weak relative to the stochastic variation in current speed and direction, there are potential advantages to longer larval durations that relate to greater growth and survival in pelagic versus benthic habitats, but not necessarily for the dispersal they facilitate (Burgess et al. 2016;Meyer et al. 2021a;Iwasa et al. 2022). There is a large literature on the evolution of marine reproductive strategies based on egg size-number trade-offs, where egg size affects larval development times depending on whether larvae feed (Vance 1973;Strathmann 1985;Emlet et al. 1987;Levitan 2000;Marshall and Keough 2007). This theory predicts that longer larval durations evolve when selection favors the production of many small offspring that feed for themselves away from adult habitat but require longer to feed and develop independently to a size and stage required for settlement back into adult habitats (Strathmann 1974(Strathmann , 1990Jackson and Strathmann 1981;Palmer and Strathmann 1981). ...
... Our goal here was to develop theory that illustrates how coastal oceanographic processes affect the evolutionary outcome of traits that affect dispersal. Most previous theory has considered reproductive strategies in the absence of oceanography (Vance 1973;Levitan 2000), considered dispersal itself as the evolving trait rather than the underlying traits of the individuals that interact with currents to give rise to dispersal patterns (Shaw et al. 2019), or focused only on larval traits (Pringle et al. 2014). We use an adaptive dynamics framework to present new theory showing how asymmetric coastal currents influence the coevolution of pelagic larval duration and adult spawning frequency in coastal ecosystems. ...
... There is empirical evidence that egg size affects pelagic larval duration depending on whether larvae feed. For feeding (planktotrophic) larvae, pelagic larval duration decreases with egg size, especially in echinoderms (Vance 1973;Emlet et al. 1987;Levitan 2000;Marshall and Keough 2007;Marshall et al. 2018). Here, we focus on feeding larvae because we are initially interested in explaining how long-distance dispersal is maintained in marine invertebrate and fish life histories and also to compare our results to previous models of pelagic larval duration in coastal oceans (e.g., Pringle et al. 2014). ...
Dispersal emerges as an outcome of organismal traits and external forcings. However, it remains unclear how the emergent dispersal kernel evolves as a by-product of selection on the underlying traits. This question is particularly compelling in coastal marine systems, where dispersal is tied to development and reproduction and where directional currents bias larval dispersal downstream, causing selection for retention. We modeled the dynamics of a metapopulation along a finite coastline using an integral projection model and adaptive dynamics to understand how asymmetric coastal currents influence the evolution of larval (pelagic larval duration) and adult (spawning frequency) life history traits, which indirectly shape the evolution of marine dispersal kernels. Selection induced by alongshore currents favors the release of larvae over multiple time periods, allowing long pelagic larval durations and long-distance dispersal to be maintained in marine life cycles in situations where they were previously predicted to be selected against. Two evolutionarily stable strategies emerged: one with a long pelagic larval duration and many spawning events, resulting in a dispersal kernel with a larger mean and variance, and another with a short pelagic larval duration and few spawning events, resulting in a dispersal kernel with a smaller mean and variance. Our theory shows how coastal ocean flows are important agents of selection that can generate multiple, often co-occurring evolutionary outcomes for marine life history traits that affect dispersal.
... Patterns of reproduction are also affected. Eggs of Caribbean fishes, echinoderms, mollusks, and bryozoans are typically larger than their corresponding taxa in the Eastern Pacific (Fig. 2D), a difference that promotes more rapid larval settlement and metamorphosis that offers advantages in the comparatively nutrient-poor and unproductive Caribbean waters (22)(23)(24)(25). Moreover, numerous Caribbean gastropods and reef corals lack planktonic development entirely and develop directly into miniature adults (26,27). ...
... Most invertebrates and fishes in strongly upwelling and highly variable environments such as the TEP produce small eggs that metamorphose into planktonic larvae that feed in the plankton for weeks to months before metamorphosis. In contrast, most species in nutrient-poor and stable environments such as the Caribbean today produce larger eggs that either metamorphose into larvae that drift for shorter intervals before metamorphosis or forgo the larval stage entirely in favor of direct maternal development of brooded young that crawl away or settle within hours to a few days of release (22)(23)(24)(25)(26)48) (Fig. 2D). Asexual (clonal) development is also more common in highly productive environments (49,50). ...
Isolation of the Caribbean Sea from the tropical Eastern Pacific by uplift of the Isthmus of Panama in the late Pliocene was associated with major, taxonomically variable, shifts in Caribbean biotic composition, and extinction, but inferred causes of these biological changes have remained elusive. We addressed this through falsifiable hypotheses about how independently determined historical changes in oceanographic conditions may have been responsible. The most striking environmental change was a sharp decline in upwelling intensity as measured from decreases in intra-annual fluctuations in temperature and consequently in planktonic productivity. We then hypothesized three general categories of biological response based upon observed differences in natural history between the oceans today. These include changes in feeding ecology, life histories, and habitats. As expected, suspension feeders and predators became rarer as upwelling declined. However, predicted increases in benthic productivity by reef corals, and benthic algae were drawn out over more than 1 Myr as seagrass and coral reef habitats proliferated; a shift that was itself driven by declining upwelling. Similar time lags occurred for predicted shifts in reproductive life history characteristics of bivalves, gastropods, and bryozoans. Examination of the spatial variability of biotic change helps to understand the time lags. Many older species characteristic of times before environmental conditions had changed tended to hang on in progressively smaller proportions of locations until they became extinct as expected from metapopulation theory and the concept of extinction debt. Faunal turnover may not occur until a million or more years after the environmental changes ultimately responsible.
... In general, large egg sizes and the high fecundity of marine invertebrates are known to be mutually exclusive due to limited resources (Vance, 1973;Hart, 1995). Therefore, there has always been a trade-off between egg size and the number of offspring in the course of life-history evolution (Strathmann and Strathmann, 1982;Hart, 1995;Podolsky and Strathmann, 1996;Levitan, 2000;Moran, 2004). More specifically, the benefits of increasing egg size include shortened planktonic larval period and an increased fertilization rate, while the cost of a large egg includes additional resources that need to be supplied for larval development, resulting in reduced fecundity. ...
The quantity of eggs produced in an annual reproductive cycle of some commercially important shellfish is vital in a hatchery operation or managing the wild populations. The horse clam Tresus keenae (Kuroda & Habe, 1950) is one of the aquaculture candidate bivalve species occurring on the subtidal soft bottom of the coastal Northwest Pacific ocean, while their reproductive effort is yet to be determined. Unlike fishes, assessing the reproductive effort of a marine bivalve is challenging since most species do not have a separable gonad except scallops, as ovaries or testis are inseparable from the visceral mass. Therefore, we developed an indirect enzyme-linked immunosorbent assay (ELISA) to measure the quantity of the egg produced in an annual reproductive cycle. The rabbit anti-egg protein IgG developed in this study was sensitive enough to detect as little as 0.3 μg/ml of the egg protein in indirect ELISA. The horse clam produced as much as 41.1% of the total body weight as eggs during spawning in October, equivalent to 378.2 million mature eggs. Histology revealed that T. keenae has a short resting period in January and February and a long period of gonial mitosis from March to August. The annual reproductive cycle and reproductive capacity of T. keenae estimated in this study provide crucial information in the successful hatchery operation to develop the horse clam aquaculture and manage the wild population for sustainable exploitation.
... An intermediate pattern known as facultative planktotrophy (Chia, 1974;Emlet, 1986;Vance, 1973a), where larvae are not only capable of feeding in the plankton but can also complete metamorphosis without food, is a rare but persistent mode of development that has been observed at least eight times across several marine invertebrate taxa (Table 1; see also Allen & Pernet, 2007). Facultative planktotrophy is often considered an intermediate mode of development in the evolutionary transition between feeding and nonfeeding larvae, but whether or not intermediate modes can maximize reproductive success over evolutionary timescales is still up for debate (Christiansen & Fenchel, 1979;Levitan, 2000;McEdward, 1997;Vance, 1973aVance, , 1973b. Larvae with facultative planktotrophy provide an opportunity to test the effects of larval feeding on several aspects of early life history, including planktonic duration, percent metamorphosis, juvenile size, and energetic reserves in juveniles. ...
Most marine invertebrate larvae either obligately feed or depend on maternally provided reserves during planktonic development. A small number of species have the capacity to do both, in a mode of development known as facultative planktotrophy. We describe facultative feeding in a larva from the Oregon coast, and identify it as being an undescribed species in the genus Amphiodia, which we refer to as Amphiodia sp. opaque. We quantified the effects of food on larval and juvenile quality by culturing larvae, collected as embryos, with and without microalgal food at 15°C. The resulting juveniles were monitored under conditions of starvation. A cohort of juveniles of larvae caught as plankton was subjected to the same starvation treatment for comparison with our laboratory-reared larvae. We observed benefits to offspring that received food: larvae provided with microalgae developed more quickly and metamorphosed at higher rates. Furthermore, juveniles resulting from fed larvae were larger and were able to avoid starvation for longer after metamorphosis. Our results varied across two experimental years, suggesting that provisions provided by parents vary between populations and years. Juveniles from planktonic larvae exhibited sizes not statistically different from larvae cultured in the absence of food, but died from starvation more quickly.
... In reef corals, an inverse relationship between egg size and temperature (Rass' rule), corresponding to a latitudinal gradient, was not supported by our findings at the interspecific level. Although temperature influences biological rates and acts as an important environmental filter, with the potential for selection and evolution of egg size (Levitan, 2000), we did not find a significant relationship between egg size and SST. Nevertheless, minor changes in egg size in response to relatively small changes in temperature can be correlated with high maternal cost in the development of offspring (Anderson & Gillooly, 2020;Marshall et al., 2020). ...
Aim
The aims were to test the role of temperature in latitudinal patterns of egg size and investigate maternal investment trade‐offs among coral taxa.
Location
Global, from 34° S to 34° N.
Time period
1981–2020.
Major taxa studied
Reef coral species from the order Scleractinia.
Methods
We compiled a comprehensive geo‐referenced global dataset of egg sizes (diameter or volume) and fecundity (number of eggs per area) for colonial corals (Scleractinia; 123 species, 5359 observations and 39 localities), substantially enhanced by new field collections (>88% of observations). We used Bayesian phylogenetic multilevel models to test for Rass' rule (a hypothesized negative relationship between egg size and temperature); we also included other environmental variables and life history traits. We also tested whether a trade‐off exists between egg size and fecundity in broadcast spawning hermaphroditic corals with horizontal symbiont transmission (HHT).
Results
We found a significant relationship between coral egg size and symbiont transmission. Eggs from coral species with vertical symbiont transmission were c . 18.8% smaller than those from species with horizontal symbiont transmission. We also found non‐significant relationships between egg size and sea surface temperature (SST) for broadcast spawning corals and between egg size and fecundity specifically for HHT species.
Main conclusions
Contrary to recognized latitudinal patterns of egg size across taxa, our study does not provide support for Rass' rule in corals. Additionally, our findings do not support a maternal investment trade‐off between egg size and fecundity for HHT species. Our study used a phylogenetic framework that should be a standard practice when studying interspecific variation, including investigation of maternal investment and identification of the influence of multiple predictors on larval fitness (egg size), in addition to trade‐offs affecting propagule influx (fecundity). Both these functional traits are vital and have direct consequences for population maintenance and connectivity in sessile organisms, such as corals.
... Egg quality, often estimated as lipid content, clearly is an important effector of larval success (Gallager & Mann 1986, Powell et al. 2002. Egg size is an important energetic tradeoff relative to larval survival (Gallager & Mann 1986, Levitan 2000, Powell et al. 2011b). Cost of reproduction as measured by mortality rate is also higher in females; thus, increased size might be advantageous in improving overall fitness for females. ...
The ocean quahog, Arctica islandica (Linnaeus 1767), is a commercially important species along the western Atlantic continental shelf. It is a long-lived species, frequently reaching ages over 200 y. Uniquely, it is one of the few bivalves to display sexual dimorphism, in that females grow to sizes larger than those of males. This phenomenon is believed to occur because males reach sexual maturity before females and, thus, have slower growth rates earlier. The growth rates of A. islandica from four sites across the Mid-Atlantic Bight, Georges Bank, Long Island (LI), and north and south of the Hudson Canyon, were measured to determine patterns in growth between males and females. Females begin to outgrow males between the ages of 5 and 15 y at sizes 5055 mm, though this varies amongst the sites and between decades. Each of the sites is unique in some way, but three sex-dependent growth dynamics are observed. Most commonly, the two sexes diverge in size with females outpacing males in growth rates after the first 515 y of life. This outcome occurs at all sites and is generally the most common outcome across decades. In a few cases, female growth rates outpace the males very early in ontogeny. Such cases occur at two sites north of Hudson Canyon, both on the LI continental shelf. Most rarely, the two sexes maintain similar growth rates. This is observed for a few decades at the most southern site. In the population as a whole, these rare outcomes have limited influence on the population so that female-to-male ratio consistently increases with increasing size. This sexually dimorphic growth is not caused by protandry, nor is it compensation for a differential mortality rate between the sexes. Cases where males grow as fast as females may be just as easily indicative of a constraint on female growth as a facilitation on male growth. Egg sizes in A. islandica are larger than those of most other bivalves with planktotrophic larvae. Accordingly, another viable hypothesis is that differential growth is an adaptation to support the large egg sizes in females, where larger female size is essential to counterweigh the consequent reduced fecundity due to larger egg volume.
Anthropogenic climate change has increased the frequency and intensity of marine heatwaves that may broadly impact the health of marine invertebrates. Rising ocean temperatures lead to increases in disease prevalence in marine organisms; it is therefore critical to understand how marine heatwaves impact immune system development. The purple sea urchin ( Strongylocentrotus purpuratus ) is an ecologically important, broadcast-spawning, omnivore that primarily inhabits kelp forests in the northeastern Pacific Ocean. The S. purputatus lifecycle includes a relatively long-lived (~2 months) planktotrophic larval stage. Larvae have a well-characterized cellular immune system that is mediated, in part, by a subset of mesenchymal cells known as pigment cells. To assess the role of environmental temperature on the development of larval immune cells, embryos were generated from adult sea urchins conditioned at 14 °C. Embryos were then cultured in either ambient (14 °C) or elevated (18 °C) seawater. Results indicate find that larvae raised in an elevated temperature were slightly larger and had more pigment cells than those raised at ambient temperature. Further, the larval phenotypes varied significantly among genetic crosses, which highlights the importance of genotype in structuring how the immune system develops in the context of the environment. Overall, these results suggest that developmental temperature shapes the larval immune system and may adversely affect survival long-term.
Organisms with external fertilization exhibit a variety of reproductive modes, from simple parthenogenesis to isogamy, anisogamy and oogamy. Here, we develop a mathematical model that helps to explain the evolution of these modes through the co-evolution of cell size and fertilization rate. By assuming that gametes can develop parthenogenetically should they fail to fertilize, and that survival of a propagule (zygote/unfertilized gamete) depends on size, we find that an isogamous population can evolve to anisogamy through evolutionary branching. Oogamy can then evolve from an anisogamous population under sexual conflict. Furthermore, we derive analytic results on the model parameters required to arrest evolution on this isogamy-oogamy trajectory. Low fertilization rates stabilise isogamy, while low fertilization costs stabilise anisogamy. Additionally we show using adaptive dynamics that isogamy can be maintained as a bet-hedging strategy in a stochastically switching environment.
Graphical Abstract
Highlights
Adapting the classic Parker-Baker-Smith model for the evolution of anisogamy (gametic sex cells of differing sizes), we provide the first analysis of the co-evolution of fertilization rate and gamete cell mass in organisms that can reproduce both sexually and asexually through parthenogenesis.
We identify a novel mechanism by which oogamy (motile microgametes and sessile macrogametes) can be selected for, arising from sexual conflict between microgametes (sperm) and macrogametes (eggs).
We identify a novel mechanism by which a state of isogamy (equal sized gametes) can be stabilized under evolution, resulting from a bet-hedging strategy in switching environments.
For all of the above insights, we develop a mathematical analysis with predictions that are supported by detailed computational simulations.
Assortative mating, where individuals non-randomly mate with respect to phenotype or genotype, can occur when preferences between potential mates have evolved. When such mate preferences occur in a population it can drive evolutionary and phenotypic divergence. But the extent to which assortative mating, mate preference, and development are evolutionarily linked remains unclear. Here we use Streblospio benedicti, a marine annelid with a rare developmental dimorphism, to investigate if mate-choice could contribute to developmental evolution. For S. benedicti two types of ecologically and phenotypically similar adults persist in natural populations, but they give rise to distinctly different offspring with alternative life-histories. This dimorphism persists despite the absence of post-zygotic reproductive barriers, where crosses between the developmental types can produce phenotypically intermediate offspring. How this life-history strategy evolved remains unknown, but assortative mating is a typical first step in evolutionary divergence. Here we investigate if female mate-choice is occurring in this species. We find that mate preferences could be contributing to the maintenance of alternative developmental and life-history strategies.
Organisms with external fertilisation exhibit a broad range of reproductive modes, from simple parthenogenesis to sexual reproduction encompassing isogamy, anisogamy, and oogamy, and including environmentally-mediated facultative sex. Here we develop a unifying mathematical model which explains the emergence of these modes via the coevolution of fertilization rate and cell size. Using a minimal assumption that survival is dependent on cell mass, and by carefully accounting for biological and evolutionary time scales, we find two distinct evolutionary outcomes: high fertilization rate (obligate sexuality) is selected when costs to cell fusion are low, while zero fertilization rate (obligate asexuality) is selected for when these costs are high. Surprisingly, in high fertilization rate scenarios evolving populations can transition from isogamy to anisogamy and oogamy via evolutionary branching. Furthermore, in variable environments we show that, without phenotypic plasticity, intermediate fertilization rates and isogamy can be maintained through bet-hedging. Allowing phenotypic plasticity can give rise to facultative sex; sexual reproduction in harsh environmental conditions, and asexuality in more benign conditions. These results parsimoniously explain a large range of empirically observed parthenogen reproduction strategies, and offer an hypothesis for the origin of binary cell fusion, a key step in the evolution of syngamy and sexual reproduction itself.
Several scenarios exist for the origin of the unusual echinoid order Clypeasteroida. The most probable of these modles is expanded here by performing a phylogenetic analysis on three clypeasteroid suborders, the enigmatic fossil genus Togocyamus, and the extinct Oligopygoida. This analysis shows that the oligopygoids are the sister group of the Clypeasteroida plus Togocyamus. The latter is here considered a plesion (extinct sister group) to the crown group Clypeasteroida. Within that order, the suborder Clypeasterina is the sister group to the Laganina plus Scutellina. A new classification of all these taxa is presented. -from Author
Larvae of two species of sea urchins (Strongylocentrotus droebachiensis and S. purpuratus) differ in initial form and in the rate of development. To determine whether these differences are attributable to the large interspecific difference in egg size, we experimentally reduced egg size by isolating blastomeres from embryos. The rate of development of feeding larvae derived from isolated blastomeres was quantified using a novel morphometric method. If the differences early in the life histories of these two species are due strictly to differences in egg size, then experimental reduction of the size of S. droebachiensis eggs should yield an initial larval form and rate of development similar to that of S. purpuratus. Our experimental manipulations of egg size produced three clear results: 1) smaller eggs yielded larvae that were smaller and had simpler body forms, 2) smaller eggs resulted in slower development through the early feeding larval stages, and 3) effects of egg size were restricted to early larval stages. Larvae from experimentally reduced eggs of the larger species had rates of development similar to those of the smaller species. Thus, cytoplasmic volumes of the eggs, not genetic differences expressed during development, account for differences in larval form and the rate of form change. This is the first definitive demonstration of the causal relationship between egg size (parental investment per offspring) and life-history characteristics in marine benthic invertebrates.
Species with large eggs and nonfeeding larvae have evolved many times from ancestors with smaller eggs and feeding larvae in numerous groups of aquatic invertebrates and amphibians. This change in reproductive allocation and larval form is often accompanied by dramatic changes in development. Little is known of this transformation because the intermediate form (a facultatively feeding larva) is rare. Knowledge of facultatively feeding larvae may help explain the conditions under which nonfeeding larvae evolve. Two hypotheses concerning the evolutionary loss of larval feeding are as follows: (1) large eggs evolve before modifications in larval development, and (2) the intermediate form (facultatively feeding larva) is evolutionarily short-lived. I show that larvae of a heart urchin, Brisaster latifrons, are capable of feeding but do not require food to complete larval development. Food for larvae appears to have little effect on larval growth and development. The development, form, and suspension feeding mechanism of these larvae are similar to those of obligate-feeding larvae of other echinoids. Feeding rates of Brisaster larvae are similar to cooccurring, obligate-feeding echinoid larvae but are low relative to the large size of Brisaster larvae. The comparison shows that in Brisaster large egg size, independence from larval food, and relatively low feeding rate have evolved before the heterochronies and modified developmental mechanisms common in nonfeeding echinoid larvae. If it is general, the result suggests that hypotheses concerning the origin of nonfeeding larval development should be based on ecological factors that affect natural selection for large eggs, rather than on the evolution of heterochronies and developmental novelties in particular clades. I also discuss alternative hypotheses concerning the evolutionary persistence of facultative larval feeding as a reproductive strategy. These hypotheses could be tested against a phylogenetic hypothesis.
Many life-history and developmental studies of marine invertebrates assume that eggs of species with nonfeeding larvae are large because they provide materials for rapid development. Using the sea urchin Heliocidaris erythrogramma which has 400 μm eggs and nonfeeding larvae, we removed an acellular, lipid-rich component from the blastula equivalent to ca. 40% of the egg volume and ca. 50% of the organic mass. Experimentally manipulated, reduced-lipid larvae survived well, developed in the usual time (3.5 d), and high percentages of the original numbers metamorphosed into anatomically normal juveniles. Control juveniles were larger at metamorphosis, grew more, and survived longer than siblings that lacked this lipid-rich material. Moderate increases in egg size in species with nonfeeding larvae may enhance postlarval performance significantly and therefore may reflect selection on early juvenile traits. The contrasts of our results and comparable experiments with feeding larvae suggests that egg size may play fundamentally different roles in species with feeding and nonfeeding larvae. The accommodation of materials reserved for the juvenile stage should be considered among hypotheses on evolutionary modification of developmental patterns.
Among marine benthic organisms, the ability to disperse, primarily during the larval stage, is widely thought to influence the extent of species geographic range. Because related species often differ in their modes of larval development (pelagic, feeding larvae; pelagic, nonfeeding larvae; or brooded development), and these can have dramatically different planktonic intervals, the mode of development may influence geographic range. A global survey of 215 regular echinoids shows that species with pelagic, feeding larvae have significantly larger ranges than those with pelagic, nonfeeding larvae, but there is no difference in ranges between species with pelagic, nonfeeding larvae and those with brooded development. These patterns are maintained within the Cidaroida and the Temnopleuroida, which account for the great majority of species with pelagic, nonfeeding development and brooded development. This limited effect of developmental mode on geographic range is found among species occurring predominantly in waters shallower than 100 m. For species occurring deeper than 100 m, there is no significant difference in geographic range related to type of development. The relationship between developmental mode and species range was examined more closely for circa 30 species for which the developmental period was known from laboratory observations. Adjusting the developmental times to a common temperature, 20°C, using realistic values for Q10 from 2.0 to 3.6, showed a highly significant, negative correlation between egg volume and developmental time, indicating the potential for developmental mode to influence the planktonic interval. However, there was no relationship between time in the plankton, estimated from unadjusted developmental times, and extent of species geographic range. These results suggest that developmental mode may influence extent of species geographic ranges indirectly through the consequences of dispersal for gene flow or recovery from disturbance.
Evolutionary biologists generally invoke male competition and female choice as mechanisms driving sexual selection. However, in broadcast-spawning organisms sperm may be limiting and females may compete, in the Darwinian sense, for increased mating success. In this study, I investigate how species differences in egg and sperm traits result in different patterns of fertilization among three closely related sea urchins (Strongylocentrotus purpuratus, S. franciscanus, and S. droebachiensis). Field studies demonstrate that all three species achieve similar percentages of eggs fertilized when eggs and sperm are released simultaneously. However, when sperm must disperse before encountering eggs, differences arise among species such that those with the smaller eggs and faster but shorter-lived sperm achieve relatively fewer fertilizations than do species with larger eggs and slower but longer-lived sperm. A field hybridization experiment, field estimates of sperm dispersal, correlations of egg size to field rates of fertilization, laboratory studies of fertilization kinetics, and a simulation model all suggest that it is attributes of the egg (probably egg size) that are responsible for the differences. These patterns of fertilization match the species' patterns of dispersion; species that do well only when sperm and eggs are released in close proximity are more aggregated, species that do relatively well when sperm and eggs are released farther apart are more dispersed. These results are consistent with the notion that eggs of different species are adapted to maximize reproductive success under different degrees of sperm limitation and suggest that male competition and female choice may not be an appropriate dichotomy in broadcast-spawning organisms.