Dataset Information

Gamete plasticity in a broadcast spawning marine invertebrate.

ABSTRACT: Sperm competition has classically been thought to maintain anisogamy (large eggs and smaller sperm) because males are thought to maximize their chance of winning fertilizations by trading sperm size for number. More recently it has been recognized that sperm quality (e.g., size, velocity) can also influence sperm competition, although studies have yielded conflicting results. Because sex evolved in the sea, debate has continued over the role of sperm competition and sperm environment in determining both sperm and egg size in externally fertilizing broadcast spawners. Remarkably, however, there have been no direct tests of whether broadcast spawners change the traits of their gametes depending on the likelihood of sperm competition. We manipulated the density (and thus, sperm environment) of a broadcast spawning ascidian (Styela plicata) in the field and then determined whether the phenotype of eggs and sperm changed. We found that sperm from adults kept at high density were larger and more motile than sperm from low-density adults. In vitro fertilizations revealed that sperm from high-density adults also lived longer and induced less polyspermy. Adult density also affected egg traits: eggs from high-density adults were smaller targets for sperm overall but produced larger ovicells than eggs from low-density adults. This suggests that broadcast spawning mothers balance (potentially conflicting) pre- and postzygotic selection pressures on egg size. Overall, our results suggest that sperm competition does not represent a strong force maintaining anisogamy in broadcast spawners. Instead, sperm limitation seems to select for large eggs and smaller, more numerous sperm.

SUBMITTER: Crean AJ

PROVIDER: S-EPMC2533220 | biostudies-literature | 2008 Sep

REPOSITORIES: biostudies-literature

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Gamete plasticity in a broadcast spawning marine invertebrate.

Crean Angela J AJ Marshall Dustin J DJ

Proceedings of the National Academy of Sciences of the United States of America 20080829 36

Sperm competition has classically been thought to maintain anisogamy (large eggs and smaller sperm) because males are thought to maximize their chance of winning fertilizations by trading sperm size for number. More recently it has been recognized that sperm quality (e.g., size, velocity) can also influence sperm competition, although studies have yielded conflicting results. Because sex evolved in the sea, debate has continued over the role of sperm competition and sperm environment in determin ...[more]

PMID: 18757726

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Project description:BACKGROUND:Colonial invertebrates such as corals exhibit nested levels of modularity, imposing a challenge to the depiction of their morphological evolution. Comparisons among diverse Caribbean gorgonian corals suggest decoupling of evolution at the polyp vs. branch/internode levels. Thus, evolutionary change in polyp form or size (the colonial module sensu stricto) does not imply a change in colony form (constructed of modular branches and other emergent features). This study examined the patterns of morphological integration at the intraspecific level. Pseudopterogorgia bipinnata (Verrill) (Octocorallia: Gorgoniidae) is a Caribbean shallow water gorgonian that can colonize most reef habitats (shallow/exposed vs. deep/protected; 1-45 m) and shows great morphological variation. RESULTS:To characterize the genotype/environment relationship and phenotypic plasticity in P. bipinnata, two microsatellite loci, mitochondrial (MSH1) and nuclear (ITS) DNA sequences, and (ITS2) DGGE banding patterns were initially compared among the populations present in the coral reefs of Belize (Carrie Bow Cay), Panama (Bocas del Toro), Colombia (Cartagena) and the Bahamas (San Salvador). Despite the large and discrete differentiation of morphotypes, there was no concordant genetic variation (DGGE banding patterns) in the ITS2 genotypes from Belize, Panama and Colombia. ITS1-5.8S-ITS2 phylogenetic analysis afforded evidence for considering the species P. kallos (Bielschowsky) as the shallow-most morphotype of P. bipinnata from exposed environments. The population from Carrie Bow Cay, Belize (1-45 m) was examined to determine the phenotypic integration of modular features such as branch thickness, polyp aperture, inter-polyp distance, internode length and branch length. Third-order partial correlation coefficients suggested significant integration between polypar and colonial traits. Some features did not change at all despite 10-fold differences in other integrated features. More importantly, some colonial features showed dependence on modular features. CONCLUSION:Consequently, module integration in gorgonian corals can be shifted, switched or canalized along lineages. Modular marine organisms such as corals are variations on a single theme: their modules can couple or decouple, allowing them to adapt to all marine benthic environments.

Project description:The hologenome theory of evolution (HTE), which is under fierce debate, presupposes that parts of the microbiome are transmitted from one generation to the next [vertical transmission (VT)], which may also influence the evolution of the holobiont. Even though bacteria have previously been described in early life stages of corals, these early life stages (larvae) could have been inoculated in the water and not inside the parental colony (through gametes) carrying the parental microbiome. How Symbiodinium is transmitted to offspring is also not clear, as only one study has described this mechanism in spawners. All other studies refer to incubators. To explore the VT hypothesis and the key components being transferred, colonies of the broadcast spawner species Mussismilia hispida were kept in nurseries until spawning. Gamete bundles, larvae and adult corals were analyzed to identify their associated microbiota with respect to composition and location. Symbiodinium and bacteria were detected by sequencing in gametes and coral planula larvae. However, no cells were detected using microscopy at the gamete stage, which could be related to the absence of those cells inside the oocytes/dispersed in the mucus or to a low resolution of our approach. A preliminary survey of Symbiodinium diversity indicated that parental colonies harbored Symbiodinium clades B, C and G, whereas only clade B was found in oocytes and planula larvae [5 days after fertilization (a.f.)]. The core bacterial populations found in the bundles, planula larvae and parental colonies were identified as members of the genera Burkholderia, Pseudomonas, Acinetobacter, Ralstonia, Inquilinus and Bacillus, suggesting that these populations could be vertically transferred through the mucus. The collective data suggest that spawner corals, such as M. hispida, can transmit Symbiodinium cells and the bacterial core to their offspring by a coral gamete (and that this gamete, with its bacterial load, is released into the water), supporting the HTE. However, more data are required to indicate the stability of the transmitted populations to indicate whether the holobiont can be considered a unit of natural selection or a symbiotic assemblage of independently evolving organisms.

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Dataset Information

Gamete plasticity in a broadcast spawning marine invertebrate.

Publications

Gamete plasticity in a broadcast spawning marine invertebrate.

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