Crenicichla adaptive radiations: parallel and non-parallel evolution of trophic-associated ecomorphs
Modified (simplified) from Burress et al. 2017. Proceedings B.
Pike cichlids (Crenicichla) fascinate me because they have, in part, forgone the classic rule book for diversification among river-dwelling organisms where most rivers and their resident assemblages consist of representatives from most major lineages. This patterns arises in riverine radiations because the vein-like branching pattern of river basins plays a central role in disrupting gene flow and ultimately isolating populations that eventually emerge as distinct allopatric species distributed in different rivers (or at least different regions of a river basin). This is to say that the branching pattern of the rivers themselves served as the catayst during speciation events. Coupled with that some basin configurations are old and stable, whereas others are more labile, frequently providing dispersal opportunities via stream capture, then any particular lineage often becomes well dispersed across the river basins in which they inhabit and sister species are rarely found in sympatry. As I mentioned, pike cichlids have, in part, scrapped this game plan and took a page (or two) out of island biogeography literature and exhibit patterns of diversification similar to that of lake- and island-dwelling organisms such that dramatic diversification has occurred within ecosystems (i.e., rivers) among endemic lineages (rather than among ecosystems or even habitats). Further, these speciation-assembled pike cichlid assemblages consist of species that are sympatric throughout the drainages in which they occur, to the extent that I (or you!) could catch members of the entire assemblage rather easily from a single section of shore line. You would, however, have to change your bait several times to satisfy the dietary preferences of the trophic-associated ecomorphs represented within the assemblages and wade into the water to apprehend with nets the ecomorphs that prefer items not amenable to traditional fishing (i.e., molluscs and periphyton). They are all there though, swimming and even foraging in mixed species aggregations.
Meet the ecomorphs!
Molluscivore
These species predominately feed upon large fractions of bivalves and snails. They supplelemt this diet with small proportions of soft-bodied invertebrates such as caddisflies. This ecomorph is characterized by stout heads and snouts, isognathous oral jaws, and robust pharyngeal jaws that bear few, robust molariform teeth. This ecomorphs has evolved in parallel in the Uruguay and Paraná Rivers. Molluscivory occurs in approximately 5% of pike cichlids (minuano, tesay, taikyra, cyclostoma, and semifasciata); perhaps about the same, maybe slightly more frequent, than across cichlids.
Periphyton-grazer
These species predominately feed upon mixtures of periphyton, algae, and diatoms that grow on the surfaces of rock slabs in shallow water. This ecomorph is characterized by elongated, decurved snouts, and robust pharyngeal jaws that bear an array of tooth types. This ecomorph has evolved in parallel in the Uruguay and Paraná Rivers. These species are gregarious and often forage in groups. Periphyton-grazing, or any form of herbivory, does not occur in any pike cichlids. Herbivory is perhaps uncommon among Neotropical cichlids, but is commonplace among African cichlids, particularly within the vast radiations of the East African Great Lakes.
Crevice-feeder
These species predominately feed upon rock-associated invertebrates (i.e., insect larvae and crustaceans) from between, underneath, and along the surface of rocks. They supplement this diet with very small fractions of small snails, which are generally consumed whole/intact. This ecomorph is characterized by a relatively deep, tapered body, long, robust oral jaws, hypertrophied oral lips, and intermediately robust pharyngeal jaws that bear simple conical teeth. This ecomorph has evolved in parallel in the Uruguay and Paraná Rivers. Crevice-feeding, as far as can be inferred from possessing hypertrophied lips, is uncommon among cichlids, but has conspicuously arose independently in association with adaptive radiation within most major lineages, including within Lakes Tanganyika, Malawi, and Victoria, as well as Nicaraguan crater lakes, and among river-dwelling groups. No other pike cichlids exhibit hypertrophied lips beyond those that evolved in parallel in C. tuca and C. tendybaguassu; however, recent field work suggests that some populations of C. missioneira (part of the Uruguay River species flock) may develop hypertrophied lips. Currently, it is not clear if this is a polymorphism or due to hybridizaton with C. tendybaguassu.
Ancestral ecomorphs
Most pike cichlids have not evolved fancy new adaptations to capture specific foods (although, in more general terms, pike cichlids are specialized relative to other Neotropical lineages). The ancestral "ecomorph", or in other words the generic pike cichlid, is a generalist predator, has a long snout, and somewhat reduced pharyngeal jaws that bear numerous tooth types (as many as five specialized types; which reflects their generalist trophic nature - a Swiss army knife so to speak). Specialist piscivores have evolved independently in the Uruguay and Paraná Rivers, but by co-opting ancestral morphologies rather than evolving novel adaptations in parallel, or rather that the adaptations are less obvious than those that accompany the trophic-roles associated with the other ecomorphs (they tend to be slender-bodied, with long pointed snouts, and large mouths, but there is enough variability in these traits across the Crenicichla phylogeny that they are difficult to separate from ancestral states). Specialist piscivores include C. celidochilus and C. missioneira in the Uruguay River and C. iguassuensis and C. sp. Urugua-i in the Paraná River. These species are also good examples of how their convergence also extends to their color patterns: the general cryptic blotches along the flank present in all the aforementioned ecomorphs that have evolved in parallel (in C. iguassuensis and C. missioneira) as well as a striped flank (as well as in C. sp. Urugua-i and C. celidochilus). Interestingly, the striped flank is probably the ancestral condition for both species flocks, which independently adopted the cryptic blotches.
The path ahead
I have shown that similar suites of ecomorphs have evolved in parallel in the Uruguay and Paraná Rivers, based on their body and pharyngeal jaw shapes and coarse trophic guilds (PDF). Naturally, this finding has merely unlocked more questions to answer. For example, I'm interested if these ecomorphs can be classified based on the species' functional morphology, if the same genes underlie the shape changes that characterize each ecomorph, and if similar fitness gain/loss is incurred with each trophic specialization. In other words, how literally parallel are these ecomorphs? I'll plod along at these questions using a combination of functional morphometrics, comparative genomics, and lab experiments.
One of my favorite places on Earth, the Cuareim River, a major right-hand tributary to the lower Uruguay River, provides a fine example of pike cichlid habitat in which the parallel ecomorphs have evolved. Particularly, the shallow, clear water, and numerous rocks and rock slabs permit the utility of crevice-feeding, periphtyon-grazing, and molluscivory (as well as piscivory, of course). This particular site sports an assemblage of six species, four members of the Uruguay River species flock (C. celidochilus, C. missioneira, C. minuano, and C. tendybaguassu, although, C. hadrostigma is also found nearby) and two from distantly related clades (C. scottii and C. lepidota). In the photo, the left-hand bank is Brazil and the right-hand bank is Uruguay.