Genetic, morphological, and chemical divergence in the sponge genus Latrunculia (Porifera: Demospongiae) from New Zealand

We undertook a comprehensive study of Latrunculia in New Zealand to determine the relationship between taxonomic, environmental, and chemical variation within the genus. Sponges were collected from five locations around New Zealand: Three Kings Islands, Tutukaka, Wellington, Kaikoura, and Doubtful Sound. Allozyme electrophoresis at nine polymorphic loci indicated that sponges from each geographic location were genetically distinct, and that they displayed genetic differences of the magnitude usually associated with reproductively isolated species (Nei's D between locations =0.375-2.476). Additionally, the comparisons revealed that the green and brown colour morphs of Latrunculia that are sympatric at Three Kings Islands and Kaikoura are distinct from each other, and that there are two genetic groups within the green sponges in Doubtful Sound. On the basis of genetic data we conclude that there are at least eight species of Latrunculia in New Zealand waters, not one to four as had been previously thought. Morphological comparisons of the eight genetic species based on skeletal characters (i.e. skeletal organisation of the choanosome, spicule composition, size, and geometry) indicated that the eight Latruncidia species fell into only two morphological groups that could be easily diagnosed on the basis of discorhabd type. Within these two primary morphological groups, skeletal characteristics among the eight species largely overlap and are not diagnostic. These findings emphasise the limitations of traditional taxonomic methods based solely on skeletal characters for distinguishing species of Latruncidia. However, multivariate analysis (MANOVA and CDA) based on six measured skeletal variables did reveal significant morphological variation among the species (Pillai's Trace=3.28, F=6.90, P<0.0001), supporting the division of the genus into eight species. Comparisons of chemical extracts from Latruncidia also showed that the amounts of five different bioactive compounds (discorhabdins A, B, C, D, and J) varied predictably among the eight species. This finding suggests that discorhabdin variation within Latrunculia, previously thought to be associated with intra-specific environmental variability, is more likely to reflect differences among species rather than phenotypic plasticity. Our results also highlight the importance of thorough taxonomic studies associated with marine natural products research to understand fully the variation in bioactive properties among individuals. The potential processes underlying the unusually high speciation rates in New Zealand Latrunculia that are indicated in our study are discussed.