Lock, Stock and Two Different Barrels: Comparing the Genetic Composition of Morphotypes of the Indo-Pacific Sponge Xestospongia testudinaria

Abstract

The giant barrel sponge Xestospongiatestudinaria is an ecologically important species that is widely distributed across the Indo-Pacific. Little is known, however, about the precise biogeographic distribution and the amount of morphological and genetic variation in this species. Here we provide the first detailed, fine-scaled (<200 km2) study of the morphological and genetic composition of X . testudinaria around Lembeh Island, Indonesia. Two mitochondrial (CO1 and ATP6 genes) and one nuclear (ATP synthase β intron) DNA markers were used to assess genetic variation. We identified four distinct morphotypes of X . testudinaria around Lembeh Island. These morphotypes were genetically differentiated with both mitochondrial and nuclear markers. Our results indicate that giant barrel sponges around Lembeh Island, which were all morphologically identified as X . testudinaria , consist of at least two different lineages that appear to be reproductively isolated. The first lineage is represented by individuals with a digitate surface area, CO1 haplotype C5, and is most abundant around the harbor area of Bitung city. The second lineage is represented by individuals with a predominantly smooth surface area, CO1 haplotype C1 and can be found all around Lembeh Island, though to a lesser extent around the harbor of Bitung city. Our findings of two additional unique genetic lineages suggests the presence of an even broader species complex possibly containing more than two reproductively isolated species. The existence of X . testudinaria as a species complex is a surprising result given the size, abundance and conspicuousness of the sponge.

Globally intertwined evolutionary history of giant barrel sponges

“…Unfortunately, this large and important animal group has long been understudied in coral reef ecology (Diaz and Rützler 2001). Most genetic studies of sponges have indicated the existence of cryptic species and refuted oceanwide distributions of several taxa (Duran and Rützler 2006;Swierts et al 2013;Bell et al 2014;Knapp et al 2015). However, these studies were done at small spatial scales, and, to the best of our knowledge, there has been no global phylogenetic study of any sponge taxon.…”

“…Xestospongia muta occurs in the tropical Atlantic, X. testudinaria in the Indo-Pacific from the Red Sea to Taiwan and X. bergquistia is thought to be confined to inshore environments in northern Australia where it lives in sympatry with X. testudinaria. Recent molecular studies have suggested that these species delineations are incorrect and that both X. muta and X. testudinaria consist of multiple sympatric species that apparently do not interbreed (Swierts et al 2013;Bell et al 2014). This has important implications for a number of published studies on the demography and population genetics of giant barrel sponges which assumed a single population of giant barrel sponge (López-Legentil and Pawlik 2009;McMurray et al 2010;Richards et al 2016).…”

“…Nuclear DNA (nDNA) evolves independently from mitochondrial DNA (mtDNA); thus, congruent patterns across these markers support the existence of biological species (Goetze 2010;Padial et al 2010). In sponges, mitochondrial variation is typically low (Wörheide et al 2005), but previous studies of giant barrel sponges have shown that the combination of the adenosine triphosphate synthase subunit 6 gene (ATP6) with the I3-M11 partition of the cytochrome oxidase 1 gene (CO1) was informative (Rua et al 2011;Swierts et al 2013). The nuclear adenine triphosphate synthesis-b intron (ATPsb) is very variable in giant barrel sponges, and because it is unlinked to the mtDNA, it serves as a good additional marker to identify potential species (Bentlage and Wörheide 2007;Swierts et al 2013).…”

“…For example, some haplotypes of the I3-M11 partition of the CO1 gene are shared between Indonesia (X. testudinaria) and Florida (X. muta); hence, two individuals from different ocean basins can be more closely related for this slowly evolving gene than two sympatric individuals on the same reef (Swierts et al 2013;Setiawan et al 2016). Giant barrel sponges from the tropical Atlantic and the Indo-Pacific sharing the same CO1 haplotype have both been related to an exterior morphology consisting of digitate structures (López-Legentil and Pawlik 2009;Swierts et al 2013). These studies imply that the giant barrel sponge is a classic example of a tropical marine animal in which poor identification at the species level has led to an oversimplified taxonomic classification.…”

Molecular biodiversity of Red Sea demosponges

“…In turn, the application of molecular tools led to the discovery of numerous cryptic species, species complexes and high degrees of endemism in sponges (e.g., Wörheide et al, 2008a;Pöppe et al, 2010;Reveillaud et al, 2010;Xavier et al, 2010;Reveillaud et al, 2011;Swierts et al, 2013). …”