Philip O. Yund

Male Reproductive Success in Sessile Invertebrates: Competition for Fertilizations

Recent in situ fertilization studies of free spawning and brooding marine organisms have focused almost exclusively on the yield of fertilized ova (female repro- ductive success). As a consequence, we know little about the factors that determine male reproductive success. If marine organisms compete for fertilizations (as do many terrestrial organisms), then a males reproductive success should be reduced by the presence of other males. We tested this hypothesis via in situ experiments employing allozyme markers for both a colonial ascidian (Botryllus schlosseri) and a bryozoan (Celleporella hyalina). Under moderate density conditions, the presence of closer male-functioning colonies reduced the fertilization success of more distant males in both species. In C. hyalina, male fertilization success also increased with allocation to sperm production. In addition, selfing rates in this species were negatively correlated with the abundance of outcross sperm. These results suggest that male reproductive success in sessile marine invertebrates must be assessed as a function of the gamete output and spatial distribution of other males in a population, and that the performance of isolated males may yield overestimates of male fertilization success in natural populations.

THE EFFECT OF SPERM COMPETITION ON MALE GAIN CURVES IN A COLONIAL MARINE INVERTEBRATE

The shape of the function that describes the relationship between resource allocation to sperm production and resulting male fertilization success (the male gain curve) plays a central role in models of sex allocation in hermaphrodites. A variety of ecological factors are expected to affect the shape of this function. Although male gain curves and male allocation patterns have been assayed in a variety of different organisms, there have been few attempts to determine whether the shape of the gain curve changes with ecological conditions. I assayed male gain curves in experimental populations of a colonial ascidian in which I manipulated the intensity of sperm competition to test the hypothesis that gain curves would saturate in the absence of competitors, but remain linear when males competed for fertilizations. Allozyme markers were utilized for paternity assignment. Results supported theoretical predictions, with the gain curve becoming progressively more linear as the intensity of sperm competition increased. Increased levels of sperm competition also had the effect of decreasing male fertilization success at all sperm production levels. These results have a number of evolutionary implications. First, the existence of a saturating gain curve under some experimental conditions provides support for the hypothesis that diminishing gains in fertilization success via male function may favor the evolution of hermaphroditism. Secondly, the changing shape of this function with ecological conditions suggests that increased allocation to sperm production should be favored in high-density populations, where sperm competition is more intense. Finally, since male fertilization success only continued to increase with sperm production when competitors were present, this suggests that high levels of sperm production in some free-spawning marine invertebrates may be in part due to the selective pressures imposed on allocation patterns by sperm competition.

Remarkable Longevity of Dilute Sperm in a Free-Spawning Colonial Ascidian

Many benthic marine invertebrates reproduce by releasing sperm into the sea (free-spawning), but the amount of time that sperm are viable after spawning may have different consequences for fertilization, depending on the type of free-spawner. In egg-broadcasting marine organisms, gamete age is usually assumed to be irrelevant because of the low probability of contact between dilute sperm and egg. However, direct dilution effects might be reduced in egg-brooding free-spawners that filter dilute sperm out of the water column, and sperm longevity may play a role in facilitating fertilization in these taxa. We investigated the effects of time, temperature, and mixing on the viability of naturally released sperm of the colonial ascidian Botryllus schlosseri. Our data indicate that B. schlosseri sperm have a functional life span that is considerably longer than those of the sperm of many other marine invertebrate taxa (half-life of ∼16 to 26 h), are able to fertilize eggs at extremely low external sperm concentrations (ca. 101 sperm ml−1), and have a longevity that varies with temperature. It is possible that such prolonged sperm longevity may be achieved by reductions in motility, reactivation of quiescent sperm by chemical cues, or intermittent swimming.

Comparison of Gamete Compatibility Between Two Blue Mussel Species in Sympatry and in Allopatry

Recent demonstrations of positive selection on genes controlling gamete compatibility have resulted in a proliferation of hypotheses concerning the sources of selection. We tested a prediction of one prominent hypothesis, selection to avoid hybridization (i.e., reinforcement), by comparing heterospecific gamete compatibility in two Mytilus edulis populations: one population in Cobscook Bay, Maine, in which the close congener, M. trossulus, is abundant (a region of sympatry), and one population in Kittery, Maine, in which M. trossulus is absent (a region of allopatry). Three diagnostic nuclear DNA markers were used to identify mussels to species and to estimate the frequency of both species and their hybrids in the two populations. Controlled crosses were then conducted by combining eggs of M. edulis females with a range of M.edulis and M. trossulus sperm concentrations. Results were not consistent with the reinforcement hypothesis. M. edulis females collected from the region of sympatry were no more incompatible with M. trossulus males than were M. edulis females collected from the region of allopatry. A trend in the opposite direction, toward greater compatibility in sympatry, suggests that introgression of M. trossulus genes that control egg compatibility, such as those encoding receptors for sperm, may influence evolution of gametic isolation in hybridizing populations.

Natural selection on hydroid colony morphology by intraspecific competition

Previous work on colonial hydroids in the genus Hydractinia has demonstrated that colony morphology is highly variable and determines intraspecific competitive ability. Competitive encounters are known to be common in nature, suggesting that intraspecific competition may be a major selective force acting on morphological variation. A replicated common garden experiment demonstrated a genetic basis to morphological variation and two data sets provided correlative support for the hypothesis of selection by intraspecific competition. First, morphologies inferior in competitive ability were less abundant in two adult, postcompetition, samples than in juvenile, precompetition, samples from the same populations. Second, among eight populations, the relative frequency of different morphologies was correlated with the frequency of intraspecific competition observed in each population. The direction of selection by competition on the morphological variation present in this species conflicts with recent predictions based on surveys across diverse taxa, suggesting limitations to the inference of competition as a past selective agent on the basis of present day correlations among species.

The role of food limitation in lobster population dynamics in coastal Maine, United States, and New Brunswick, Canada

Abstract Lobster (Homarus americanus) landings in Maine, United States have increased steadily over the past two decades to levels that are consistently more than triple the 40‐year (1950 to 1990) annual average of c. 9000 MT. Meanwhile, the use of herring (Clupea harengus) as bait has increased fourfold since the 1970s, and is currently subsidising lobster productivity in mid‐coast Maine by augmenting the diet and growth of large juvenile and young adult lobsters before they recruit to the fishery. We investigated whether herring bait in the eastern portions of the Gulf of Maine is also subsidising these lobster populations. In 2004, we compared stomach contents, tissue production via stable isotope ratios, and growth rates of lobsters from seasonally open (Cutler, Maine, United States) and closed (Dipper Harbour, New Brunswick, Canada) fishing areas in the spring, summer, and autumn. Contrary to previous results in mid‐coast Maine, lobsters from seasonally closed sites at Dipper Harbour outgrew those from fished sites around Cutler. Yet examination of the diet of lobsters revealed several differences between open and closed sites that did not exist at sites in mid‐coast Maine. For instance, lobsters at Dipper Harbour consumed markedly more bivalves than those at Cutler. Furthermore, quantification of trap densities and the number of licensed fishers in mid‐coast versus eastern Maine determined that fishing effort was greatly reduced in eastern Maine. Thus, our results indicate thatherring bait subsidies are not important in eastern portions of the Gulf of Maine, but the availability of natural prey seemingly limits the growth of lobsters in eastern Maine. Moreover, our study suggests that bottom‐up forcing (i.e., food limitation) can have important consequences for lobster population dynamics and the productivity of lobster fisheries.

The effect of variation in population density on male fertilization success in a colonial ascidian

Abstract Past investigations of the effect of variation in population density on fertilization processes under field conditions have focused entirely on the consequences for female fertilization success (the proportion of eggs fertilized). In contrast, we explored the effects of population size and density on male fertilization success (proportion of embryos fathered or eggs fertilized by individual males) via an in situ density manipulation that utilized allozyme markers to assay paternity after fertilization had occurred. Male-phase ascidian colonies in high density experimental populations experienced competition for fertilizations, which reduced the ability of a focal male to fertilize eggs brooded by individual female colonies. However, the concomitant increase in the number of females with eggs available to be fertilized offset this decline. Consequently, the overall, population-wide fertilization success of focal males did not vary between density treatments. Although population density did not affect the quantitative fertilization success of male colonies, an increase in the genetic diversity of offspring may nevertheless confer a fitness advantage to both males and females that reproduce in higher density populations.

Across-shelf transport of bivalve larvae: can the interface between a coastal current and inshore waters act as an ecological barrier to larval dispersal?

Using an integrated physical and biological approach, we examined across-shelf advection and exchange and the associated transport of bivalve larvae in the presence of a strong coastal current separated from the coast by a stratified inshore environment. We tested the hypothesis that the interface of the coastal current and inshore waters can act as an ecological barrier to across-shelf transport of larvae but can be overcome by wind- or tidally-induced transport. Our study region in the Gulf of Maine encompasses a coastal current that diverges from the coast as it moves downshelf. The region inshore of this current is home to several species that exhibit limited recruitment in spite of extensive upshelf larval sources. Analysis of surface water temperatures and wind velocities revealed episodic decreases in temperature along the coast correlated with alongshelf (but not upwelling) winds, indicating wind-forced onshore movement of the cold coastal current. Such wind-driven onshore migrations are more common along the northern portion of the study region where the coastal current is near the coast, tidal currents are strong, and wind directions are more conducive to onshore migration, but rarer further south where the interface between inshore waters and the coastal current is further offshore and suitable wind events are less common. The distribution of bivalve larvae was consistent with the physical measurements. There was little across-shelf variation in larval abundance where the current abuts the coast, indicating strong across-shelf exchange of larvae, but strong across-shelf variation in larval density where the stratified inshore waters separate the current from the coast, indicating weak across-shelf transport of larvae. Our results suggest that the interface between the coastal current and inshore waters may constitute a major ecological barrier to larval dispersal in the southern part of the region that may only be overcome by rare, strong wind-forced events.

Evolutionary Genetics of the Hydroid Allodeterminant alr2

We surveyed genetic variation in alr2, an allodeterminant of the colonial hydroid Hydractinia symbiolongicarpus. We generated cDNA from a sample of 239 Hydractinia colonies collected at Lighthouse Point, Connecticut, and identified 473 alr2 alleles, 198 of which were unique. Rarefaction analysis suggested that the sample was near saturation. Most alleles were rare, with 86% occurring at frequencies of 1% or less. Alleles were highly variable, diverging on average by 18% of the amino acids in a predicted extracellular domain of the molecule. Analysis of 152 full-length alleles confirmed the existence of two structural types, defined by exons 4-8 of the gene. Several residues of the predicted immunoglobulin superfamily-like domains display signatures of positive selection. We also identified 77 unique alr2 pseudogene sequences from 85 colonies. Twenty-seven of these sequences matched expressed alr2 sequences from other colonies. This observation is consistent with pseudogenes contributing to alr2 diversification through sequence donation. A more limited collection of animals was made from a distant, relict population of H. symbiolongicarpus. Sixty percent of the unique sequences identified in this sample were found to match sequences from the Lighthouse Point population. The large number of alr2 alleles, their degree of divergence, the predominance of rare alleles in the population, their persistence over broad spatial and temporal scales, and the signatures of positive selection in multiple residues of the putative recognition domain paint a consistent picture of negative-frequency-dependent selection operating in this system. The genetic diversity observed at alr2 is comparable to that of the most highly polymorphic genetic systems known to date.

EFFECTS OF FERTILIZATION DISTANCE ON MALE GAIN CURVES IN A FREE‐SPAWNING MARINE INVERTEBRATE: A COMBINED EMPIRICAL AND THEORETICAL APPROACH

Male gain curves describe the relationship between allocation to sperm production and male reproductive success and are central to models of sex allocation in hermaphrodites. Sperm competition is expected to result in more linear gains and select for increased allocation. We hypothesized that high sperm production in passively mating systems may also be the result of selection to enhance the ability to fertilize distant ova. Consequently, we explored the effect of distance on male gain curves in a free-spawning colonial ascidian. The performance of focal males that varied in sperm production was assayed at three distances via microsatellite markers. An advection-diffusion model was used to estimate sperm concentration gradients, to predict male reproductive gain integrated across multiple downstream females, and explore effects of hydrodynamic conditions. As distance increased, male reproductive success decreased and empirical gain curves became increasingly linear. Our model predicted that the expected net gain curve is relatively insensitive to variation in flow regime and will saturate much more slowly than if only a single, nearby distance is considered. Thus, high levels of sperm production may enhance fitness both in competitive situations and with increasing fertilization distance, highlighting the need to consider distance effects when evaluating gain curves.