The constituents of bacterial communities, their diversity and biogeography are poorly understood and yet microbial ecology drives Earth's ecology (Curtis et al., 2002). The predominant theory in microbial diversity has been that ‘everything is everywhere, the environment selects’ (Cho and Tiedje, 2000). However, studies of bacteria in symbiotic relationships with eukaryotes and in soils are revealing that endemism exists within the microbial world and bacterial diversification is ongoing (Fulthorpe et al., 1998; Cho and Tiedje, 2000; Funk et al., 2000). Genetic data are increasingly showing that in the microbial world everything is not everywhere, suggesting that the distribution of bacteria can be restricted by factors such as distance between sites (Cho and Tiedje, 2000).
The gut of animals changes quickly from a totally sterile environment before birth to a numerous and highly diverse microbial community that is maintained throughout life (Ley et al., 2006). However, the acquisition and diversity of commensals has not been extensively studied, in part because past approaches have used culture-based techniques to identify gut communities which limits the identifications to culturable commensals (Pace, 1997). Methods for identifying microbes based on the amplification of DNA have been applied recently to the gastrointestinal flora of animals, especially humans (for example Ley et al., 2006; 2008; Palmer et al., 2007; Li et al., 2008) and are providing insights into the vast diversity and the source of these microbial commensal communities.
It is generally thought that commensals are either inherited from parents during the parental care stage or they are acquired later in life from close contacts such as mates (Brooks and McLennan, 1991), or via a combination of both routes. Thus commensal organisms can be thought of as inherited as ‘heirlooms’ or acquired as ‘souvenirs’ (Kliks, 1990). The two methods of acquiring commensals give rise to two different patterns of relationships between hosts and commensals. If commensals are perpetually inherited as heirlooms, host and commensal phylogenies will be congruent and parasite community similarity will be negatively correlated with host genetic distance; if commensals are acquired as souvenirs, host and commensal phylogenies will almost certainly be incongruent (Brooks and McLennan, 1991; Paterson and Banks, 2001) and commensal community similarity will not be correlated with host genetic similarity. If host and commensal phylogenies are incongruent, it is likely that factors other than inheritance, for example spatial proximity, explain the acquisition of commensals. Understanding the extent of transfer of faecal bacteria may also provide insight into the transmission routes potential pathogens may take.
We examined whether the faecal commensals of Adelie penguins, Pygoscelis adeliae, are souvenirs or heirlooms. Adelie penguins breed on ice-free areas around the margin of the Antarctic continent and islands south of about latitude 60°S and then disperse only as far north as the limits of the pack ice during the non-breeding season (Marchant and Higgins, 1990). Thus Adelie penguins are an ideal group in which to study the source of faecal flora as human disturbance has been very recent and limited. We cloned and sequenced a portion of the 16S rRNA gene from DNA extracted from bacterial communities obtained from faecal swabs of Adelie penguins breeding at six sites in Antarctica to identify the faecal bacteria and to examine hypotheses regarding the distribution of bacteria. We also used a DNA fingerprinting tool (automated ribosomal intergenic spacer analysis, ARISA) to characterize and compare the faecal communities of breeding birds. ARISA utilizes length variation in the intergenic spacer region between the 16S rRNA and the 23S rRNA genes, a hypervariable region that varies among species and among strains of bacteria, to characterize bacterial communities (Fisher and Triplett, 1999). ARISA is a fast and relatively inexpensive method of characterizing microbial communities and thus allows more samples to be processed compared with traditional methods (Brown et al., 2005).
We found that faecal microbial communities from individual birds were remarkably diverse and most bacterial taxa were present in only a small proportion of the birds we examined, suggesting that each bird has a unique faecal community. A few bacterial taxa were distributed over large geographic distances. We found a significant negative correlation between faecal bacterial community similarity and host genetic similarity from the clone libraries and the ARISA data. There was no support for a correlation between bacterial community similarity and distance between collection sites.