Plasticity in hatching potentially adjusts risks of benthic and planktonic development for benthic marine invertebrates. The proportionate effect of hatching plasticity on duration of larval swimming is greatest for animals that can potentially brood or encapsulate offspring until hatching near metamorphic competence. As an example, early hatching of the nudibranch mollusk Phestilla sibogae is stimulated by scattering of encapsulated offspring, as by a predator feeding on the gelatinous egg ribbon. When egg ribbons are undisturbed, hatching is at or near metamorphic competence. Disturbance of an unguarded benthic egg mass can insert 4 or more days of obligate larval dispersal into the life history. As another example, the spionid annelid Boccardia proboscidea broods capsules, each with both cannibalistic and developmentally arrested planktivorous siblings plus nurse eggs. Early hatching produces mainly planktivorous larvae with a planktonic duration of 15 days. Late hatching produces mainly adelphophages who have eaten their planktivorous siblings and metamorphose with little or no period of swimming. Mothers actively hatch their offspring by tearing the capsules, and appeared to time hatching in response to their environment and not to the stage of development of their offspring. Higher temperature increased the variance of brooding time. Females appeared to hatch capsules at an earlier developmental stage at lower temperatures. Species that release gametes or zygotes directly into the plankton have less scope for plasticity in stage at hatching. Their embryos develop singly with little protection and hatch at early stages, often as blastulae or gastrulae. Time of hatching cannot be greatly advanced, and sensory capabilities of blastulae may be limited.
All organisms face two fundamental trade-offs in the allocation of energetic resources: one between many small versus a few large offspring, and the second between present and future reproduction. Nowhere are these trade-offs more apparent than in the vast range of variation in the sizes of eggs and offspring exhibited among species of marine invertebrates. It has become increasingly clear that, in many taxa of marine organisms, there is also substantial intraspecific variation in the size of eggs and hatchings. This variation has largely been attributed to adaptive maternal effects. In theory, however, the inevitable conflicts of interest that arise in families of sexually reproducing organisms over the optimal distribution of parental resources among siblings could also account for much of this variation in egg and offspring size. Here, we explore the potential impacts of family conflict on offspring traits by comparing the life histories of two exemplar species of marine organisms, the polychaete Boccardia proboscidea and the gastropod Solenosteira macrospira, emphasizing how differences in modes of fertilization and parental care might influence the phenotype and, consequently, the fitness of offspring.
Poecilogony is the production of different larval types within the same species. Although rare, poecilogonous species are ideal systems for testing the evolutionary and ecological implication of different developmental modes in marine invertebrates. Here, we described a new case of poecilogony, the Southern Hemisphere spionid Boccardia wellingtonensis. We used a combination of common-garden experiments, video recordings, and in vitro manipulations of individuals from three sites to (1) document the type of poecilogony, the brooding behavior of the mother, and the hatching process; (2) experimentally measure the effect of nurse eggs on the growth and type of larvae produced; and (3) document variation in the length of the brooding period, number of capsules, larvae, and nurse eggs of mothers from three sites to explore the potential for plasticity in reproductive traits. These results were compared to the previously reported poecilogonous species B. proboscidea, which resembles B. wellingtonensis in size, morphology, ecology, and reproductive strategy but differs in capsule structure. We found that in contrast to B. proboscidea, B. wellingtonensis produced larvae that, in isolation and in the presence of nurse eggs, developed into a wide range of offspring sizes. Mothers brood and hatch the larvae with frequent partial hatching of the brood during the brooding period. Although larvae could not liberate themselves, larvae crossed to other capsules as interconnections between capsules broke during the developmental period, potentially affecting food availability, sibling competition for nurse eggs, and cannibalism. Variation in brooding time and number of capsules deposited among sites suggest local adaptations.
The ability to produce more than one kind of offspring, or poecilogony, is a striking example of reproductive variability. Traditionally, larval nutrition has been classified as a dichotomy: if offspring obtain nutrition from their mothers (lecithotrophy), there is lower fecundity and greater chance of offspring survival than when they get their nutrition from plankton (planktotrophy). The polychaete Boccardia proboscidea (Spionidae) produces both types of embryos using three different reproductive strategies. In this study, we examined the roles of genetic history and phenotypic plasticity on explaining natural variation in B. proboscidea along the Pacific coast of the United States using two genetic mitochondrial markers, 16S rDNA and Cyt b, and common garden experiments. These data show a single North American West Coast network that is structured, geographically, by the well-documented biogeographic break near Point Conception, California. The southern group within this network covers a smaller range, but has larger haplotype diversity, than the northern group. Some individuals differing in reproductive type had the same haplotype, indicating independence of these features; however, differences between laboratory and field data suggest additional geographic variation within one of the reproductive types. Females from higher latitudes provide offspring with larger supplies of extra embryonic nutrition than females from southern latitudes. Results herein suggest that both genetic history and developmental plasticity are playing a role in the maintenance of this reproductive polymorphism.
In poecilogony, different types of larvae are produced within the same species. Previous studies have suggested maternal control of the production of larval types; however, it is not clear which factors or mechanisms generate contrasting developmental patterns among siblings. The spionid polychaete Boccardia proboscidea produces within the same capsule adelphophagic larvae that eat nurse eggs and siblings and complete all or most of their development inside the capsule (Type A larvae), and larvae with little growth until they hatch as planktotrophic larvae (Type B larvae). In this study, we manipulated capsule content to explore the factors determining larval type in B. proboscidea and the role of extra‐embryonic maternal nutrition and sib–sib interaction in the developmental fate of offspring. When early larval stages were grown individually in vitro, with nurse eggs as the only food source, some of them remained small, while others continue developing into larger pre‐competent larvae by feeding on nurse eggs. This suggests that larval types in B. proboscidea are determined very early in development and are not solely the product of sib–sib interaction inside the capsule. However, our data also suggest that hatching size variability within larval types of a clutch depends on nurse egg availability. Type B larvae grew normally to metamorphosis when phytoplankton was available, but suffered high rates of cannibalism by Type A larvae. These results are consistent with the hypothesis that individual larval fates are determined very early in development and that once their fate is determined, hatching size and intracapsular survival are affected by maternal food provisioning and sibling interaction.
Previous studies of population genetic structure in Dissostichus eleginoides have shown that oceanographic and geographic discontinuities drive in this species population differentiation. Studies have focused on the genetics of D. eleginoides in the Southern Ocean; however, there is little knowledge of their genetic variation along the South American continental shelf. In this study, we used a panel of six microsatellites to test whether D. eleginoides shows population genetic structuring in this region. We hypothesized that this species would show zero or very limited genetic structuring due to the habitat continuity along the South American shelf from Peru in the Pacific Ocean to the Falkland Islands in the Atlantic Ocean. We used Bayesian and traditional analyses to evaluate population genetic structure, and we estimated the number of putative migrants and effective population size. Consistent with our predictions, our results showed no significant genetic structuring among populations of the South American continental shelf but supported two significant and well-defined genetic clusters of D. eleginoides between regions (South American continental shelf and South Georgia clusters). Genetic connectivity between these two clusters was 11.3% of putative migrants from the South American cluster to the South Georgia Island and 0.7% in the opposite direction. Effective population size was higher in locations from the South American continental shelf as compared with the South Georgia Island. Overall, our results support that the continuity of the deep-sea habitat along the continental shelf and the biological features of the study species are plausible drivers of intraspecific population genetic structuring across the distribution of D. eleginoides on the South American continental shelf.
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