Microscale genetic differentiation in a sessile invertebrate with cloned larvae: investigating the role of polyembryony

Abstract

Microscale genetic diVerentiation of sessile organisms can arise from restricted dispersal of sexual propagules, leading to isolation by distance, or from localised cloning. Cyclostome bryozoans oVer a possible combination of both: the localised transfer of spermatozoa between mates with limited dispersal of the resulting larvae, in association with the splitting of each sexually produced embryo into many clonal copies (polyembryony).We spatially sampled 157 colonies of Crisia denticulata from subtidal rock overhangs from one shore in Devon, England at a geographic scale of ca. 0.05 to 130 m plus a further 21 colonies from Pembrokeshire, Wales as an outgroup. Analysis of molecular variance (AMOVA) revealed that the majority (67%) of genetic variation was distributed among individuals within single rock overhangs, with only 16% of variation among diVerent overhangs within each shore and 17% of variation between the ingroup and outgroup shores. Despite local genetic variation, pairwise genetic similarity analysed by spatial autocorrelation was greatest at the smallest inter-individual distance we tested (5 cm) and remained signiWcant and positive across generally within-overhang comparisons (<4 m). Spatial autocorrelation and AMOVA analyses both indicated that patches of C. denticulata located on diVerent rock overhangs tended to be genetically distinct, with the switch from positive to negative autocorrelation, which is often considered to be the distance within which individuals reproduce with their close relatives or the radius of a patch, occurring at the 4-8 m distance class. Rerunning analyses with twenty data sets that only included one individual of each multilocus genotype (n = 97) or the single data set that contained just the unique genotypes (n = 67) revealed that the presence of repeat genotypes had an impact on genetic structuring (PhiPT values were reduced when shared genotypes were removed from the dataset) but that it was not great and only statistically evident at distances between individuals of 1-2 m. Comparisons to a further 20 randomisations of the data set that were performed irrespective of genotype (n = 97) suggested that this conclusion is not an artefact of reduced sample size. A resampling procedure using kinship coeYcients, implemented by the software package GEN-CLONE gave broadly similar results but the greater statistical power allowed small but signiWcant impacts of repeat Communicated by M. Wahl. Electronic supplementary materialThe online version of this article

Small-scale spatial genetic structure in Scopalina lophyropoda, an encrusting sponge with philopatric larval dispersal and frequent fission and fusion events

“…2), which detected the formation of pedigree structures. In contrast, clonality, which often contributes to the strong SGS at very small scales (Pemberton et al 2007, Miller & Ayre 2008, was irrelevant in Scopalina lophyropoda, since both the genet and the ramet analyses gave similar results.…”

“…corals, bryozoans and ascidians) by using autocorrelation statistics (e.g. McFadden & Aydin 1996, Miller 1998, Pemberton et al 2007, Miller & Ayre 2008. Although sponges are common components of marine systems (e.g.…”

Micro-scale genetic heterogeneity and structure in coral recruitment: fine-scale patchiness

“…In addition, evidence of self-seeding has been found in this species for the FGB (Brazeau et al 2005). It is possible that other factors may have influenced our observations of fine-scale genetic structure, including kin aggregation (Veliz et al 2006), polyembryony (Pemberton et al 2007), and selection (Zvuloni et al 2008). We cannot rule out any of these explanations; all of them, however, require additional factors beyond our suggestion of low dispersal with limited larval mixing to produce the observed patterns.…”

Does sperm supply limit the number of broods ­produced by a polyembryonous bryozoan?

“…Several circumstances have been suggested that should favour the evolution and maintenance of polyembryony in animals, but most of these do not seem applicable to algae, plants, or colonial animals, such as cyclostome bryozoans, that mate at a distance by the remote transfer of male gametes (see Pemberton et al 2007). More applicable explanations envisage polyembryony as making 'the best of a bad job' in the face of constraints on mating opportunities (Craig et al 1997).…”

“…Data from a study of Crisia denticulata failed to support a suggestion by Ryland (1996) that polyembryony might be a response to limited gene flow in sessile species in which 'potential mates will differ little, and sexual reproduction may produce larvae with genotypes no less fit within the immediate vicinity than their parent'. A large proportion of the total genetic variability encompassed by 2 widely separated populations of C. denticulata was present within patches of colonies in small-scale rock overhangs (Pemberton et al 2007); thus, potential mates would not be genetically similar. Ryland (1996) also predicted (echoing an earlier suggestion made for red algae with aflagellate gametes by Searles 1980) that low sperm output from typically small cyclostome colonies, when combined with a sparse adult distribution, gave a low probability that a colony could capture enough sperm to fertilise all the eggs it could potentially produce.…”