Population genetics at three spatial scales of a rare sponge living in fragmented habitats

Rare species have seldom been studied in marine habitats, mainly because it is difficult to formally assess the status of rare species, especially in patchy benthic organisms, for which samplings are often assumed to be incomplete and, thus, inappropriate for establishing the real abundance of the species. However, many marine benthic invertebrates can be considered rare, due to the fragmentation and rarity of suitable habitats. Consequently, studies on the genetic connectivity of rare species in fragmented habitats are basic for assessing their risk of extinction, especially in the context of increased habitat fragmentation by human activities. Sponges are suitable models for studying the intra- and inter-population genetic variation of rare invertebrates, as they produce lecitotrophic larvae and are often found in fragmented habitats.

We investigated the genetic structure of a Mediterranean sponge, Scopalina lophyropoda (Schmidt), using the allelic size variation of seven specific microsatellite loci. The species can be classified as "rare" because of its strict habitat requirements, the low number of individuals per population, and the relatively small size of its distribution range. It also presents a strong patchy distribution, philopatric larval dispersal, and both sexual and asexual reproduction. Classical genetic-variance-based methods (AMOVA) and differentiation statistics revealed that the genetic diversity of S. lophyropoda was structured at the three spatial scales studied: within populations, between populations of a geographic region, and between isolated geographic regions, although some stochastic gene flow might occur among populations within a region. The genetic structure followed an isolation-by-distance pattern according to the Mantel test. However, despite philopatric larval dispersal and fission events in the species, no single population showed inbreeding, and the contribution of clonality to the population makeup was minor (only ca. 4%).

The structure of the S. lophyropoda populations at all spatial scales examined confirms the philopatric larval dispersal that has been reported. Asexual reproduction does not seem to play a relevant role in the populations. The heterozygote excess and the lack of inbreeding could be interpreted as a hitherto unknown outcrossing strategy of the species. The envisaged causes for this strategy are sperm dispersal, a strong selection against the mating of genetically related individuals to avoid inbreeding depression or high longevity of genets combined with stochastic recruitment events by larvae from other populations. It should be investigated whether this strategy could also explain the genetic diversity of many other patchy marine invertebrates whose populations remain healthy over time, despite their apparent rarity.