Intraspecific divergence in sperm morphology of the green sea urchin, Strongylocentrotus droebachiensis: implications for selection in broadcast spawners

<p>Abstract</p> <p>Background</p> <p>Sperm morphology can be highly variable among species, but less is known about patterns of population differentiation within species. Most studies of sperm morphometric variation are done in species with internal fertilization, where sexual selection can be mediated by complex mating behavior and the environment of the female reproductive tract. Far less is known about patterns of sperm evolution in broadcast spawners, where reproductive dynamics are largely carried out at the gametic level. We investigated variation in sperm morphology of a broadcast spawner, the green sea urchin (<it>Strongylocentrotus droebachiensis</it>), within and among spawnings of an individual, among individuals within a population, and among populations. We also examined population-level variation between two reproductive seasons for one population. We then compared among-population quantitative genetic divergence (<it>Q</it>_ST) for sperm characters to divergence at neutral microsatellite markers (<it>F</it>_ST).</p> <p>Results</p> <p>All sperm traits except total length showed strong patterns of high diversity among populations, as did overall sperm morphology quantified using multivariate analysis. We also found significant differences in almost all traits among individuals in all populations. Head length, axoneme length, and total length had high within-male repeatability across multiple spawnings. Only sperm head width had significant within-population variation across two reproductive seasons. We found signatures of directional selection on head length and head width, with strong selection possibly acting on head length between the Pacific and West Atlantic populations. We also discuss the strengths and limitations of the <it>Q</it>_ST-<it>F</it>_STcomparison.</p> <p>Conclusion</p> <p>Sperm morphology in <it>S. droebachiensis </it>is highly variable, both among populations and among individuals within populations, and has low variation within an individual across multiple spawnings. Selective pressures acting among populations may differ from those acting within, with directional selection implicated in driving divergence among populations and balancing selection as a possible mechanism for producing variability among males. Sexual selection in broadcast spawners may be mediated by different processes from those acting on internal fertilizers. Selective divergence in sperm head length among populations is associated with ecological differences among populations that may play a large role in mediating sexual selection in this broadcast spawner.</p

Restriction Site Tiling Analysis: accurate discovery and quantitative genotyping of genome-wide polymorphisms using nucleotide arrays

A method for the simultaneous identification of polymorphic loci and the quantitative genotyping of thousands of loci in individuals is presented

Postmating Female Control: 20 Years of Cryptic Female Choice

Cryptic female choice (CFC) represents postmating intersexual selection arising from female-driven mechanisms at or after mating that bias sperm use and impact male paternity share. Although biologists began to study CFC relatively late, largely spurred by Eberhard's book published 20 years ago, the field has grown rapidly since then. Here, we review empirical progress to show that numerous female processes offer potential for CFC, from mating through to fertilization, although seldom has CFC been clearly demonstrated. We then evaluate functional implications, and argue that, under some conditions, CFC might have repercussions for female fitness, sexual conflict, and intersexual coevolution, with ramifications for related evolutionary phenomena, such as speciation. We conclude by identifying directions for future research in this rapidly growing field

Whole-Genome Positive Selection and Habitat-Driven Evolution in a Shallow and a Deep-Sea Urchin

Comparisons of genomic sequence between divergent species can provide insight into the action of natural selection across many distinct classes of proteins. Here, we examine the extent of positive selection as a function of tissue-specific and stage-specific gene expression in two closely-related sea urchins, the shallow-water Strongylocentrotus purpuratus and the deep-sea Allocentrotus fragilis, which have diverged greatly in their adult but not larval habitats. Genes that are expressed specifically in adult somatic tissue have significantly higher dN/dS ratios than the genome-wide average, whereas those in larvae are indistinguishable from the genome-wide average. Testis-specific genes have the highest dN/dS values, whereas ovary-specific have the lowest. Branch-site models involving the outgroup S. franciscanus indicate greater selection (ωFG) along the A. fragilis branch than along the S. purpuratus branch. The A. fragilis branch also shows a higher proportion of genes under positive selection, including those involved in skeletal development, endocytosis, and sulfur metabolism. Both lineages are approximately equal in enrichment for positive selection of genes involved in immunity, development, and cell–cell communication. The branch-site models further suggest that adult-specific genes have experienced greater positive selection than those expressed in larvae and that ovary-specific genes are more conserved (i.e., experienced greater negative selection) than those expressed specifically in adult somatic tissues and testis. Our results chart the patterns of protein change that have occurred after habitat divergence in these two species and show that the developmental or functional context in which a gene acts can play an important role in how divergent species adapt to new environments

Multiple mechanisms of cryptic female choice act on intraspecific male variation in Drosophila simulans

Postcopulatory sexual selection can arise when females mate with multiple males and is usually mediated by an interaction between the sexes. Cryptic female choice (CFC) is one form of postcopulatory sexual selection that occurs when female morphology, physiology, or behavior generates a bias in fertilization success. However, its importance in nonrandom reproductive success is poorly resolved due to challenges distinguishing the roles of females and males in generating patterns of fertilization bias. Nevertheless, two CFC mechanisms have recently been documented and characterized in Drosophila simulans within the context of gametic isolation in competitive hybrid matings with Drosophila mauritiana: sperm ejection and nonrandom use of sperm storage organs for fertilization. Here, we explore if and how female D. simulans employ these two mechanisms of CFC in response to intraspecific male size variation. We used transgenic males expressing green (GFP) or red fluorescent protein (RFP) in sperm heads to document postcopulatory processes, in conjunction with a probabilistic analytical model. We unexpectedly found that differential reproductive success was also a function of male population (GFP or RFP), suggesting that females use different CFC mechanisms to select for different male traits. Moreover, concordance of selection at the precopulatory (as measured by mating latency) and postcopulatory stages depends on both the male trait and the CFC mechanism examined. Larger males were more successful both before and after mating, but we unexpectedly found that females also mated more quickly with males with GFP-labeled sperm, while fertilization bias favored RFP-labeled sperm.peerReviewe

Data from: An analytical framework for estimating fertilization bias and the fertilization set from multiple sperm-storage organs

How sperm from competing males are used to fertilize eggs is poorly understood, yet has important implications for postcopulatory sexual selection. Sperm may be used in direct proportion to their numerical representation within the fertilization set or with a bias toward one male over another. Previous theoretical treatments have assumed a single sperm-storage organ, but many taxa possess multiple organs or store sperm within multiple regions of the reproductive tract. In Drosophila, females store sperm in two distinct storage organ types: the seminal receptacle (SR) and the paired spermathecae. Here, we expand previous 'raffle' models to describe 'fertilization bias' independently for sperm within the SR and the spermathecae and estimate the fertilization set based on the relative contribution of sperm from the different sperm-storage organ types. We apply this model to three closely related species to reveal rapid divergence in the fertilization set and the potential for female sperm choice

How female × male and male × male interactions influence competitive fertilization in Drosophila melanogaster

How males and females contribute to joint reproductive success has been a long-standing question in sexual selection. Under postcopulatory sexual selection (PSS), paternity success is predicted to derive from complex interactions among females engaging in cryptic female choice and males engaging in sperm competition. Such interactions have been identified as potential sources of genetic variation in sexually selected traits but are also expected to inhibit trait diversification. To date, studies of interactions between females and competing males have focused almost exclusively on genotypes and not phenotypic variation in sexually selected traits. Here, we characterize within- and between-sex interactions in Drosophila melanogaster using isogenic lines with heritable variation in both male and female traits known to influence competitive fertilization. We found surprisingly few genotypic interaction effects on various stages of PSS such as female remating interval, copulation duration, sperm transfer, or sperm storage. Only the timing of female sperm ejection depended on female × male genotypic interactions. By contrast, several reproductive events, including sperm transfer, female sperm ejection and sperm storage, were explained by two- and three-way interactions among sex-specific phenotypes. We also documented complex interactions between the lengths of competing males’ sperm and the female seminal receptacle, which are known to have experienced rapid female-male co-diversification. Our results highlight the non-independence of sperm competition and cryptic female choice and demonstrate that complex interactions between the sexes do not limit the ability of multivariate systems to respond to directional sexual selection

Data from: No evidence for postcopulatory inbreeding avoidance in Drosophila melanogaster

Selection to avoid inbreeding is predicted to vary across species due to differences in population structure and reproductive biology. Over the past decade, there have been numerous investigations of postcopulatory inbreeding avoidance, a phenomenon that first requires discrimination of mate (or sperm) relatedness and then requires mechanisms of male ejaculate tailoring and/or cryptic female choice to avoid kin. The number of studies that have found a negative association between male-female genetic relatedness and competitive fertilization success is roughly equal to the number of studies that have not found such a relationship. In the former case, the underlying mechanisms are largely unknown. The present study was undertaken to verify and expand upon a previous report of postcopulatory inbreeding avoidance in D. melanogaster, as well as to resolve underlying mechanisms of inbreeding avoidance using transgenic flies that express a sperm head-specific fluorescent tag. However, siblings did not have a lower fertilization success as compared to unrelated males in either the first (P1) or second (P2) mate role in sperm competition with a standard unrelated competitor male in our study population of D. melanogaster. Analyses of mating latency, copulation duration, egg production rate and remating interval further revealed no evidence for inbreeding avoidance

Number of progeny and sperm in storage for D. mauritiana

NA indicates no data. For methods and analysis, see Manier, M.K., J.M. Belote, S. Lüpold, K.S. Berben, O. Ala-Honkola, W.F. Collins and S. Pitnick. 2013. Rapid diversification of sperm precedence traits and processes among three sibling Drosophila species. Evolution in press.; Manier, M.K., J.M. Belote, K.S. Berben, D. Novikov, W.T. Stuart and S. Pitnick. 2010. Resolving mechanisms of competitive fertilization success in D. melanogaster. Science 328: 354-357. Variables: N1 – number of progeny sired by the first male to mate. N2 - number of progeny sired by the second male to mate. SR1 – number of first-male sperm in the SR. SR2 – number of second-male sperm in the SR. Sp1 – number of first-male sperm in both spermathecae combined. Sp2 – number of second-male sperm in both spermathecae combine