What we really know about the diversity of Clownfish
Clownfish are a recent example of an adaptive radiation that occurred within the tropical oceans of the Indo-Pacific. Their adaptation to associate with anemones allowed rapid diversification across the region following the acquisition of a new resource. Recent work resolving the relationships among clownfish has helped biologists understand more about how speciation occurs in the marine environment. While some classical assumptions remain true, others have been challenged. We also finally have an idea of how the first clownfish might have looked and behaved, and how certain physical characteristics among the group have changed over time.
Clownfish underwent their initial formation around 15 - 20 million years ago in the ‘bulls eye of diversity’ that is the Indo-Australian Archipelago (IAA). This initial event was followed by a geographical replicate as ancestors to the African clownfish crossed the Indian Ocean and reached the coast of Madagascar and Southeast Africa around 4 million years ago. These fishes were able to exploit new regions of habitable reef environments. The African coast, Arabian Peninsula, and finally the Red Sea, are the furthest geographic areas inhabited by clownfish, and species indigenous to these areas are some of the most derived (recently evolved).
Figure 1: The evolutionary tree of clownfish is displayed and color mapped based on geographic location of each species. The African clade is shown independently with associated anemone hosts. The classic complexes are also shown, like complexes are outlined in color-coded boxes.
So what exactly do the clownfish ‘complexes’ really mean?
Recently, the most comprehensive phylogenetic analysis (evolutionary relationships) of clownfish has shown that species traditionally grouped together are not necessarily more related to each other. For example, the Clarkii complex has been thought of as the largest group, encompassing over 10 different species, including: A. clarkii, A. chrysogaster, and A. chrysopterus. However, these species are much less related to each other than are A. clarkii and the Tomato clowns like A. melanopus, A. frenatus, and A. ephippium. Incongruences on all complexes were found except for the Maroon and Percula groups. However, most of these discrepancies are small, and only one or two species from each complex is out of place. In the Skunk complex, only A. nigripes is falsely included. In the Saddleback and Tomato complexes, only A. latezonatus and A. mccullochi make the clade paraphyletic (an incomplete group). Of all the complexes, it is the Clarkii group that is largely misrepresented. A more accurate analysis would group all the Clarkii variants together, perhaps the chrysopterus variants together, and the African clownfish together. Although it is easy to imagine the Clarkii complex being a complete group in the past, as clownfish as a whole have diversified, separating many of the traditionally grouped species is currently a more accurate representation.
Figure 2: A. clarkii is the most diverse species of clownfish. Many geographical variants are known to exist. Here, the polymorphisms in Japan (just a small portion of the A. clarkii home range) are displayed.
What drives speciation in clownfish?
The initial radiation was a subsequent consequence of the formation of mutualistic relationships with their host sea anemones, and it has been posited that ecological speciation is responsible for current diversity. However, the answer to this question is largely unknown. Ecological speciation is where different environments lead to the creation of reproductive barriers. Once isolated, populations diverged due to genetic isolation and the specific selective pressures of a particular geographic area. This is rare in the marine world, as the environment is more contiguous than terrestrial counterparts. In this example, a clownfish will find a new isolated area and then diversify, a pattern reoccurring over and over again. This theory has gained support by the fact that the any two closely related species have very little, if any overlap of geographical habitat (termed allopatric speciation). For example, A. chagonensis and A. nigripes are both in the Indian Ocean but show little to no overlap. A. omanensis, and A. bicinctus both occur near coastal Arabia, but one, A. omanensis is restricted to the Oman coast, while A. bicinctus occurs primarily in the Red Sea. And again, A. chrysogaster, A. allardi, and A. latifiasciatus are strictly African in distribution, but have minimal range overlap. So while some species are not geographically isolated in present day, it is probable that those species were spatially isolated as each formed in the past independently.
However, ecological speciation predictions do not explain all of the diversity within the clownfish group. Another study has shown that variants of A. clarkii cluster by color and not by geographic location. Individuals sharing melanistic traits are more closely related than individuals of differing traits in the same region. This contradicts the ecological speciation model, which would predict close geographic relatives to be more closely related. Clarkii clownfish are peculiar in behavior. They are the only documented species to survive without an anemone host, they have also been shown to be bigamous as opposed to monogamous. This is largely attributed to their low dependence on host anemones, and in some areas, a shortened breeding season. More work exploring the causes of speciation in clownfish is needed and this will likely involve genomics and big data analysis.
Figure 3: This is a beautiful example of the diversity with the Clarkii group. This is an Australian variant. (Photo Credit: Peter Martis)
The origins of clownfish
The radiation of clownfish has been an intriguing area of study as it has disabused some classic adaptive theoretical assumptions. Evolutionary theory suggests that the original ancestor should be a generalist, and as it diversified becomes more and more specialized into different habitats and behavioral patterns. However, the most generalist clownfish, A. clarkii, is large bodied, a ubiquitous user of anemone hosts, and bold in behavior. A. clarkii is neither the most ancestral, nor the most derived of the clownfish, but instead is and intermediary within the group. Mapping physical characteristics with phylogenetic analysis allows the resolution of how certain characteristics change over time. Physical features such as the number of bars, body depth, caudal fin shape (truncated or rounded), host dependence, and number of hosts, have all been explored to explain how the ancestral clownfish looked and behaved.
The first clownfish was likely a slender, elongated, and small bodied fish with a rounded caudal fin. Prior to their mutualistic relationship with anemones, the predecessor to clownfish hid within rocks of the reefs and was timid in behavior. After the mutualism occurred, this slender small-bodied fish associated with more than one host anemone. Following this association, there are some apparent shifts in character traits over time and across the different species. Anemone hosts are extremely efficient in protection, as is evident by the 30-year lifespan of clownfish, over 6 times longer than what would be expected in comparable species. Following this appearance of a trait allowing for new interactions where the fish are well protected, there is a trend toward large bodied, better swimming fish. Across time we see more and more deep bodied clownfish, and more emargination of the caudal fin. This is likely in response to changes in feeding behavior. As fish ventured further and further from their anemone hosts for feeding opportunities, they became better and better swimmers. Deep bodies, and emarginated caudal fins are adaptive to better swimming. There is also a trend towards a loss of bars. It is likely that the ancestral clownfish had 3 bars, as is evident in P. biaculeatus, A. percula, and A. ocellaris. Unlike the trends in deeper bodies and caudal fin emargination, there is not really an explanation for the loss of bars, and this remains a mystery.
Lord Howe Island presents an interesting example of how the co-occurrence of two separate species in a single geographic area can occur. Lord Howe is positioned almost 400 miles off the southeast coast of Australia and is one of the most isolated of all the geographical areas containing clownfish; it is the southern tip of the Amphiprion range and has been colonized by two species separately. First, A. latezonatus, and second A. mccullochi. Although these species both inhabit this isolated area, they are very distally related. A. latezonatus is closely related to the ocellaris/percula group and has a very basal position within Amphiprions as a whole, while A. mccullochi is more derived and likely came over from the eastern coast of Australia where its close relative A. akindynos occurs. As is the pattern across clownfish as a whole, when two species occur in the same area, there tends to be a trend towards differential host preference. In Lord Howe, latezonatus prefers Heteractis crispa as a host, while A. mccullochi prefers Entacmaea quadricolor.
Clownfish have proven to be an exciting group to study how rapid diversification can occur following the acquisition of new resources. In this case, the resource was protection from their extremely efficient anemone hosts. Following the initial formation of the group, there was another diversification as A. chrysogaster like clownfish reached the east coasts of Madagascar and Africa. Recent research has parsed out most of the evolutionary relationships among the different species and how clownfish as a whole have changed over time. Clownfish are very diverse in both physical shape, and behavior, and one of the most exciting aspects of husbandry within the clownfish family is understanding where each species comes from geographically, and how it fits in among all the others.
Figure 4: The origins of the clownfish A. thiellei remain uncertain. This species is thought to be a continually occurring hybrid (two thiellei have never been seen as a pair in the wild), and it often pairs with A. ocellaris in the wild.
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