Phylogeny and Kleptoplasty
The opisthobranchs are an extremely diverse group, having undergone impressive adaptive radiation and striking parallel evolution, making the resolution of phylogenetic relationships quite difficult [27,28]. Approximately nine orders are currently recognised, including the sacoglossa, nudibranchia and anaspidea (the sea hares) [27]. Recent studies have attempted to overcome the difficulties in resolving phylogenetic relationships by using various methods of molecular analysis to elucidate these phylogenies [28-30], but even with these methods there has been some disagreement as to the placement of the more basal groups [27-29].
It is currently thought that both the sacoglossa and the anaspidea arose from within the cephalaspidea (the headshield slugs), and that the diaphanidae, a family of marine snails and slugs, is the most likely precursor group [27,30]. The diaphanidae are, however, paraphyletic and so it is currently unclear as to which exact lineage gave rise to these groups [27,30]. A close evolutionary relationship between the sacoglossa and the cephalaspidea is not such a stretch to imagine, as the less derived sacoglossans, specifically the Ascobulla and Cylindrobulla, are not dissimilar anatomically from the cephalaspidea [27-31]. The Ascobulla are shelled sacoglossans possessing a uniserial radula and ascus sac, as seen in the more derived sacoglossans, though appear more similar morphologically to the basal Cylindrobulla [27]. Ascobulla live in the sediment, that is, they are infaunal. Accepting that parallel evolution is far more likely than complex re-emergence, it can be assumed that this is a plesiomorphic trait which further confirms their basal position within the sacoglossa [28]. The gizzard, a key functional characteristic of the cephalaspidea, has been lost in the sacoglossa as a result of their feeeding specialisation [27].
The loss of a shell has occurred numerous times throughout the mollusca, particularly within the gastropods and most strikingly within the cephalopods. Within the sacoglossa only the larvae are shelled in most groups, though those groups which are considered to be more basal (namely the genera Ascobulla and Cylindrobulla) have retained their protective shells [27]. Given the numerous times snails have evolved into slugs, it is clear that something has been driving this evolutionary trend, but what? The answer may come in the form of secondary metabolites, synthesised from their algal prey, found to be present in non-shelled sacoglossans and used as a kind of chemical armoury. There is evidence that indicates there is more than just a correlation between the production of chemical defences and the reduction or disappearance of a shell in the evolutionary history of the opisthobranchs [27,31]. Faulker and Ghiselin presented evidence that these chemical defences evolved within the sacoglossa whilst shells, or mechanical defences, were still in place [27,31]. It is likely that the evolution of chemical defence was the precursor that drove shell reduction in the sacoglossa, thereby allowing further biological changes to occur in these animals that ultimately lead to their unique kleptoplastic capability [27,31].
The origin of kleptoplasty, a trait unique to the sacoglossa, is perhaps surprisingly poorly studied given its likely evolutionary implications. A recent study by Maeda and colleagues on the molecular phylogeny of the group aimed to address this dearth of information, finding that the origin of kleptoplasty can likely be traced to the uptake and retention of non-functional chloroplasts at the base of the sacoglossa, along with the evolution of suctorial feeding [28]. It has only evolved into functional kleptoplasty in the Plakobranchacea, specifically within the Plakobranchoidea, which includes the Elysiidae [28]. Based on the available data, they concluded that it seemed likely non-functional kleptoplasty was secondarily lost in the three shelled genera Ascobulla, Cylindrobulla and Volvatella, as indicated by Figure 1 below [28]. Whilst highly plausible, there are some issues with this theory that highlight the difficulty in resolving the phylogenies of this group. Firstly, the authors proposed that the reasoning behind this secondary loss of kleptoplasty was a shift from epifaunal to infaunal environments [28], whilst it has been suggested by other authors that an infaunal lifestyle is the ancestral condition, and not a reversion in these groups [27]. Secondly, if the phylogeny presented in this study (and seen in Figure 1 below) is an accurate representation of the evolutionary history of kleptoplasty, then it is would seem somewhat baffling that it would evolve in the common ancestor of these lineages only for it to be secondarily lost in all three in such a short evolutionary time frame. Regardless of the potential flaws in this theory, it is clear that the evolution of kleptoplasty has had a profound impact on the evolutionary trajectory of the sacoglossa, and is well deserving of further study.
Figure 1- Phylogenetic relationships within the Sacoglossa based on nuclear (18S rRNA) and mitochondrial (CO1, trnV and 16S rRNA) gene sequences. Bold lines represent groups where kleptoplasty is seen. The black arrow denotes the likely evolutionary origin of kleptoplasty, while the white arrow denotes the loss of kleptoplasty. Adapted from Maeda et al, 2010 [29]. Note: functional kleptoplasty in seen only in the Plakobranchacea, which includes the Elysiidae. |