Long Branches and Phylogenetic Diversity

A measure of a species' expected contribution to genetic, or evolutionary distinctiveness is derived from its position in a phylogeny that can be used to place a value on that taxon (see chapters in this book). And as all life on earth has a common ancestor (Darwin 1859; Theobald 2010), we can consider the phylogenetic value of any species in the context of the whole (Fig. 4). This view of life based on DNA sequences of full genomes reveals that phylogenetic diversity is dominated by microscopic organisms and conservation of any visible life (fungi, plants, animals) preserves very little evolutionary distinctiveness (Fig. 4; Ciccarelli et al. 2006). Thus, as a starting point in the application of phylogenetics to conservation we should put equal resources into maintaining diversity within the three major lineages (or long branches): Bacteria, Archaea and Eukarya. However, the only species we know sufficiently well to recognise a decline and have knowledge to remedy are eukaryotes. In addition, it is the habitats provided by multicellular organisms that

Fig. 4 Phylogenetic diversity on Earth is dominated by microscopic organisms, as revealed by the tree of life based on 31 universal protein families (Redrawn from Ciccarelli et al. 2006). Branch lengths give an indication of the extent of diversity and lineage age. Note the very shallow branches among popular large creatures (red clade). Some of the more widely known microbes are labelled but every branch represents a distinct taxon

we have invested resources into studying; habitats that host numerous interesting lineages of Bacteria and Archaea (Eckburg et al. 2005).

Thousands of low-abundance taxa account for most of the observed phylogenetic diversity in any environment. This “rare biosphere” contains a large proportion of phylogenetic diversity and represents an enormous contribution to genetic distinctiveness and evolutionary innovation (Sogin et al. 2006; Nee 2004a). After Anton von Leeuwenhoek first looked at bacteria in lake water and material scraped from his teeth in the seventeenth century, our understanding and appreciation of the distribution and abundance of microorganisms advanced relatively slowly. It is now accelerating rapidly as technological developments allow us to obtain and analyse large amounts of DNA data directly from environmental samples containing large numbers of taxa (Lozupone and Knight 2008). Indeed the current state of technology means that microbial genomes are tractable objects for whole genome sequencing. We will soon know whether the 4957 bacterial taxa found in soil of a commercial apple orchard (Shade et al. 2012) is species rich (but phylogenetically restricted) compared to a marine plankton net sample with 189 species of zooplankton (Machida et al. 2009), or human skin with more than 205 species of bacteria from 19 phyla (Grice et al. 2009). Microbial phenotype arrays allow the gathering of far more precise ecological detail about bacteria than is available for eukaryotes (Bochner 2008). There is also emerging evidence of additional fundamental types of life on Earth (Zakaib 2011).

As an example of the known unknowns, consider New Zealand sponges. Sponges are multicellular (visible) marine animals of the phylum Porifera. In coastal water around New Zealand 733 species of sponges have been recorded from 20 orders (Kelly et al. 2006). As with much of the New Zealand fauna (see Trewick and Morgan-Richards 2009), about 95 % of these are endemic to the region at the species level. However, in themselves these species contribute little directly to global diversity because other closely related species exist elsewhere. Generally sponges are not endangered, although special regions of high diversity that exist in hydrothermal areas and on seamounts are under pressure from benthic trawling (Kelly et al. 2006, and see Gianni 2004).

Nevertheless conservation of any sponge species or even population contributes much more; sponges are home to distinct microbial communities (microbiomes) so the total number of phyla preserved might reach more than 40. Sponges host rich microorganism communities and with next generation DNA sequencing data the number of known bacterial phyla in sponges has recently increased (Webster et al. 2010; Schmitt et al. 2012). Although many of the detected phyla are formally described, such as the Algae, Fungi, Actinobacteria, Chloroflexi (Green non-sulfur bacteria), Cyanobacteria, Nitrospira, and Proteobacteria (Fig. 5), several new ones have also been discovered in sponges (Turque et al. 2010; Webster et al. 2010; Schmitt et al. 2012). A single sponge provides an environment that protects an impressive array of phylogenetic diversity (Taylor et al. 2007). So how can we best conserve the phylogenetic diversity harboured inside sponges? Will one species or one geographic region suffice?

Fig. 5 Each sponge is home to a community of microscopic life that encompasses the range of known phylogenetic diversity on Earth. Here the major phyla found within a sponge microbiome are named on the tree of life. The sponge pictured is Raspailia topsenti, one of five sympatric sponge species studied by Schmitt et al. (2011) from New Zealand coastal waters (Phylogeny redrawn from Ciccarelli et al. 2006. Image © Katie Dowle)

Samples from eight locations around the world detected 2567 bacterial taxa representing 22 phyla living inside sponges (Schmitt et al. 2012), while three species of Australian sponge held a total of 2996 bacteria taxa from 36 phyla (Webster et al. 2010). Different sponge species from the same environment possess distinct symbiotic communities. Some components of their bacterial communities appear to be passed from parent to offspring while other components are acquired from the surrounding seawater (Webster et al. 2010; Schmitt et al. 2012). Thus, although a few bacteria are found in all sponges the majority are either host or region specific. For example tropical sponges have microbial communities that are more similar to each other than to the communities in subtropical sponges.

Schmitt et al. (2011) collected five sponge species from a single bay on the coast of New Zealand. By focusing on just the bacteria that are members of the phylum Chloroflexi they compared species diversity between sponges with either high or low microbial abundance, and contrasted this with Chloroflexi diversity in the surrounding seawater. Fifty-eight species of Chloroflexi were recorded from inside the sponges, but only three species in the seawater (Schmitt et al. 2011). About half these taxa were new to science. Ecologically important roles and specific associations of Chloroflexi bacteria were inferred for the sponge species with high microbial abundance as the majority of their bacteria fell into sponge-specific and sponge-coral phylogenetic lineages (Schmitt et al. 2011). Thus any single sponge species houses plenty of phylogenetic diversity but if we want to conserve all lineages that are restricted to sponges, we need to conserve more than one sponge species.