Speciation and phylogeography in the cosmopolitan marine moon jelly, Aurelia sp

Abstract

Background: The cosmopolitan moon jelly Aurelia is characterized by high degrees of morphological and ecological plasticity, and subsequently by an unclear taxonomic status. The latter has been revised repeatedly over the last century, dividing the genus Aurelia in as many as 12 or as little as two species. We used molecular data and phenotypic traits to unravel speciation processes and phylogeographic patterns in Aurelia.

Results: Mitochondrial and nuclear DNA data (16S and ITS-1/5.8S rDNA) from 66 world-wide sampled specimens reveal star-like tree topologies, unambiguously differentiating 7 (mtDNA) and 8 (ncDNA) genetic entities with sequence divergences ranging from 7.8 to 14% (mtDNA) and 5 to 32% (ncDNA), respectively. Phylogenetic patterns strongly suggest historic speciation events and the reconstruction of at least 7 different species within Aurelia. Both genetic divergences and life history traits showed associations to environmental factors, suggesting ecological differentiation forced by divergent selection. Hybridization and introgression between Aurelia lineages likely occurred due to secondary contacts, which, however, did not disrupt the unambiguousness of genetic separation.

Conclusions: Our findings recommend Aurelia as a model system for using the combined power of organismic, ecological, and molecular data to unravel speciation processes in cosmopolitan marine organisms.

Figure 1

Genealogy of Aurelia lineages based on 16S rDNA (a) and ITS-1/5.8S rDNA (b) sequences. The total number of mtDNA haplotypes and ncDNA alleles studied per lineage are given and their geographic origins are listed in fig. 1a (^*the Mljet lakes samples group in mitochondrial LIM lineage but constitute a new lineage in the ncDNA tree). Branch lengths are drawn from Maximum Likelihood tree searches using substitution models (mtDNA: GTR+G, -ln Likelihood 1255.44, α = 0.15; ncDNA: HKY+G, TS/TV = 0.94, α = 0.27). Fig. 1a). Bootstrap values at branches derive from 1000 MP replicates, the dotted branches are only supported in MP analysis. Numbers in parentheses represent absolute numbers of apomorphic changes (Acctran optimisation, branch & bound search, 56 informative characters, CI = 0.86, gaps were excluded). Fig. 1b). Bootstrap values are from 100 ML/1000 MP replicates, heterozygous and hybrid individuals are marked by A and B alleles; Cyanea capillata is shown to have close relationship to the Aurelia LIM lineage (for further explanations see text).

Figure 2

Geographic distribution of mitochondrial Aurelia lineages. Three main climate zones divide the lineages into cold/boreal, temperate/mediterran, and warm-tropical temperature ranges. Minimum sea temperatures averaged from all sampling locations per lineage are given in parentheses (*excluding the 4 LIM-MKL hybrid individuals from LIM lineage in Adriatic Mljet lakes due to their untypical life history traits, see discussion). The geographic origin of the tropical MCA lineage (?) is unknown.

Figure 3

Principal component analysis of 15 polyp clones attributes 74% of the total phenotypic variance (of 6 phenotypic variables) to component 1 (PC1, 59%) and component 2 (PC2, 15%). Two important traits, strobilation frequency (ephyrae symbolize number of seasons/year) and induction temperature for strobilation onset, which coincide with mtDNA lineage distribution along PC1 are depicted. Symbols for mtDNA lineages are: • BOR, ▴ LAB, ▾ UBI, □ ARAB, ▪ TET, ♦ MCA; no data exist for the LIM lineage.