The stability paradox
Ancient lakes are commonly portrayed as long-lived, isolated and relatively stable environments with low extinction rates and a steady increase in the number of species. However, upon close scrutiny, most ancient lakes reveal both steady limnological ageing processes (Mackay 1998) and complex physical/chemical histories owing to drastic geological and climatic changes. Although Lake Victoria appears to date back 750 000 years, it experienced a major regression or complete drought about 18 000–15 000 years ago. Similarly, the older Lake Malawi (4–5 Myr) and Tanganyika (9–12 Myr) experienced a coincidental severe water-level drop as recently as 135 000–75 000 years ago (Scholz et al. 2007). Lake Titicaca has also experienced major fluctuations that separated the basin into three to five small paleo-lakes during its history (Mourguiart 2000). Similarly, the geological history of the Caspian basin involves major transgressions and regressions followed by drastic changes in salinity regimes that triggered several well-documented episodes of mass extinction (Zenkevich 1963). Even Lake Baikal, the oldest, deepest and most stable of the ancient lakes, experienced notable environmental perturbations (Williams et al. 1997). Baikalian mollusc and diatom fossil data indicate that their evolution proceeded through several distinctive phases, each characterized by diverse and unique endemic faunas (Sherbakov 1999). Clearly, the fauna of ancient lakes must have been severely affected by the major changes in water levels which were associated not only with physico-chemical modifications but also with both biological stress and opportunities for population subdivision. These perturbations were often associated with major extinction waves, and it is likely that they played important roles in opening new ecological axes, making the lakes susceptible to new waves of colonization. How these factors influenced the pathway of diversification remains largely unexplored.
Colonization history, timing and tempo of radiation events
An understanding of evolutionary diversification processes benefits from clear knowledge of the evolutionary history of lineages that experienced radiations. Thus, particular consideration has been given to the ages of species flocks, the timing of their radiation, and the rate of speciation. The extremely young age of cichlid species in the African great lakes and their high speciation rate (Seehausen 2002; Won et al. 2005) has led some authors to speculate that many species flocks are very young. By contrast, there are also several assemblages, such as the gammarids, pulmonates, and possibly turbellarians of Lake Baikal, the gammarids and mysids of Caspian Lake, and the thalassoid gastropods and several cichlid tribes of Lake Tanganyika that contain lineages as old or older than the basin they inhabit, suggesting that ancient lakes may also act as long-term evolutionary reservoirs (Nishida 1991; Sherbakov et al. 1998; Salzburger et al. 2002b; Cristescu et al. 2003; Wilson et al. 2004). Assigning ages to particular group is not a trivial task, particularly when considering that most of these closely related lineages contain manifold clades of various ages resulting from a complex invasion history (Sherbakov 1999). Colonization histories of ancient lakes can vary from single events to pulse or continuous introductions over long periods of time. Continuous introductions are more probable for plankton and for benthic species with life stages adapted for high dispersal potential, whereas pulse introductions are more common for taxa with low dispersal ability. Regardless of dispersal strategy, species utilizing either continuous or pulse dispersal mechanisms have developed distinct species flocks. However, the complex invasion histories are potentially obscured even further by introgressive hybridization between closely related species (Seehausen 2004; Herder et al. 2006).
The intricate relations between the fauna of major ancient lakes and their surrounding watersheds have been examined in a historical perspective to infer the number of colonization events that have given rise to a particular species flock (Martens 1997; Macdonald et al. 2005; Elmer et al. 2009). For example, the cichlids of Lake Tanganyika are probably derived from multiple invasions that independently inaugurated radiations (Meyer 1993). Similarly, the recent Quaternary radiation of the Ponto-Caspian crustaceans (cladocerans, amphipods, mysids) that resulted in diversification at the genus level represents an extension of a diversification initiated earlier (during the Miocene, Pliocene, or Pleistocene) in the Sarmatian paleolake and seeded by multiple colonizations of both marine and freshwater ancestors (Cristescu et al. 2003; Cristescu & Hebert 2005). Examples strongly supporting monophyletic relationships indicative of one major colonization also exist. For example, large groups of cichlids in Lake Victoria and Malawi and of cottoid fishes in Lake Baikal are descended from one or a few ancestral species (Kontula et al. 2003; Verheyen et al. 2003). While the pace and geographical pattern of ancient lake radiations need to be confirmed for each studied flock, complex radiations of manifold clades suggestive of pulse diversification have been shown to be common.
The ecological and evolutionary factors that facilitate repeated colonizations followed by major, successive habitat transitions remain elusive. Kolar & Lodge (2001) propose an invasion model where species introduction and colonization face a series of selective filters based on both physical/chemical and biological characteristics of the habitat. Within this context, after a drastic ecological perturbation, an ancient lake would be less resistant to invasion with a high probability of new niches being made available. Such environmental perturbations had the potential to facilitate new waves of colonization of ancestral lineages, while also advancing further diversification of surviving resident lineages. It is easy to imagine that severe environmental perturbations also facilitate massive hybridization waves.
Interestingly, hybridization itself could play an important role in facilitating repeated colonization and parallel evolution. For example, Schluter & Conte (2009) propose the ‘transporter’ hypothesis to explain the repetitive, independent origin of freshwater stickleback species from a marine ancestral ecotype, in one of the best-documented cases of parallel evolution. The authors suggest that the derived freshwater population contributes to the standing genetic variation in the marine (ancestral) population. In this simple scenario, alleles from freshwater-adapted populations are constantly exported back to the sea by hybridization followed by introgression. The freshwater-adapted genotype disintegrates slowly through recombination while supplementing the marine gene pool with novel alleles, providing increased invasive potential to their carriers and allowing the repeated colonization of new freshwater ecosystems. The model proposed by Schluter & Conte (2009) for postglacial stickleback evolution in North America could also explain the pattern of repeated invasions in ancient lakes if lake-adapted alleles are being transported outside the main lakes via hybridization and introgression, enhancing the invasiveness of populations inhabiting the surrounding watersheds. Although appealing, this model remains to be rigorously tested in other systems.
The Malili Lake system of Central Sulawesi (Indonesia) with its three hydrologically connected lakes (Matano, Towuti and Mahalona) and complex watershed provides a good setting for testing the ‘transporter’ hypothesis. For example, the sister species of the sailfin silversides of the family Telmatherinidae possess adaptive traits (skull and jaw morphology) specific to certain local shoreline habitats, suggesting strong local adaptation, as well as conspicuous male chromatic polymorphism indicative of sexual selection (Roy et al. 2007). However, based on a multilocus phylogenetic approach, Herder et al. (2006) concluded that the group shows strong signature of hybridization (conflicting cytonuclear and intranuclear phylogenetic signal in the multilocus dataset), suggesting that the spread of adaptive alleles across the population’s distribution via introgressive hybridization may have contributed to this radiation. Interestingly, Herder et al. (2006) observed that recent hybridization occurred not only within one of the major lake clades, the Telmatherina sharpfins, but also between lake and stream telmatherinids. The number of stream/lake habitat transitions (colonizations) that seeded the radiation of telmatherinids remains obscured by the recurring hybridization events between stream and lake lineage. Nevertheless, this finding opens the possibility that key adaptive alleles could be also transported outside the main lakes via hybridization and introgression, enhancing the capacity of stream individuals to explore or colonize lake habitats.
Perhaps, the most intriguing aspect of ancient lake evolution is the rapid nature of speciation in some flocks within these systems. There is strong molecular, fossil and biogeographical evidence that many adaptive radiations in ancient lakes have occurred at a very high rate. The mean times to speciation for amphipods and sculpins in Lake Baikal have been estimated at 5–7 and 0.6–0.9 Myr, respectively, while speciation intervals for cichlids range from 0.1 to 0.3 Myr in Lake Malawi and 0.7–1.1 Myr in Lake Tanganyika (reviewed in Turner 1999; Coyne & Orr 2004). Speciation intervals for cichlids in the crater lakes Nabugabo and Barambi Mbo (0.004–0.4 Myr) and Lake Victoria (0.001–0.2 Myr) appear to be much shorter (Schliewen et al. 1994; Seehausen 2002). Overall, these values are significantly higher than the mean diversification interval of 6.5 Myr calculated by Coyne & Orr (2004) for a representative number of plants, animals and protists. Based on a comparison of 33 intralacustrine radiations and 76 nonradiations in cichlids, Seehausen (2006) documented that young radiations and earlier stages of the older radiations are characterized by high speciation rates that start declining after at least 0.5 Myr since colonization. This evidence is consistent with mathematical models (Gavrilets & Vose 2005), suggesting that speciation rates are very rapid near the time of colonization, but begin to decline as the radiation ages. Gavrilets & Losos (2009) proposed several explanations for this pattern, including the concept of ecological opportunity or the availability of niches in a particular environment. It is generally thought that at the time of colonization, there is a wide range of niches open to utilization, triggering the rapid diversification of a species to occupy these spaces. As these niches are filled, the number of opportunities is reduced and the rate of speciation plateaus or declines. Additionally, as species become more specialized, there may be greater genetic and physiological constraints that hinder further divergence and thus limit speciation rates. However, as Seehausen (2006) points out, ecological opportunity alone is not sufficient to predict the occurrence of a radiation, and thus important intrinsic factors are probably involved. Additionally, cases of nonradiation in biologically similar colonization events suggest an element of chance as well, reminding us that evolution has also a contingent component.
Parallel evolution in ancient lakes
One considerable area of study has been whether ancient lakes radiations are predictable, that is, driven by common ecological and evolutionary processes. Although various taxonomic groups have undergone adaptive radiation in different lakes (e.g. cichlid fishes in the African Great Lakes Malawi, Tanganyika and Victoria; cottoid fishes and gammarid amphipods in Lake Baikal; thalassoid gastropods in Lake Tanganyika; orestiid fishes and hyalellid amphipods in Lake Titicaca; telmatherinid fishes in the Malili lakes of Sulawesi), remarkable cases of evolutionary parallelism have been observed in unrelated species flocks from various lakes, suggesting that similar ecological and evolutionary drivers have triggered the accelerated cascade of diversification observed in many ancient lakes (Martens 1994; Fryer 1996). For example, the Cyprideis ostracods of Lake Tanganyika resemble morphologically the Cytherissa ostracods of Lake Baikal. Similar armature morphology has been observed in the acanthogammarids of Lake Baikal and the hyalellids of Lake Titicaca (reviewed in Martens 1997). The gastropods of the Malili lakes display many parallel shell and radula morphs in different lakes (von Rintelen et al. 2004). Morphologically similar species of cichlids have also evolved independently in different East African Lakes (Kocher et al. 1993; Rüber et al. 1999; Allender et al. 2003; Salzburger 2009).
Recent studies suggest that selection regimes alone owing to similar ecological context or similar female preference are not sufficient to produce these parallel morphologies (Salzburger 2009) and that intrinsic factors such as life history attributes (e.g. brooding, ovoviviparity, viviparity, breeding philopatry), develop-mental or genetic constraints (Albertson et al. 2003), as well as key morphological or physiological innovations (Liem 1973) could contribute to the observed directional diversification (reviewed in Martens 1997; Schön & Martens 2004). For example, the modification of the pharyngeal jaw apparatus (PJA) of cichlid fishes, which allows the specialized use of the oral jaw for prey capture and the pharyngeal jaw for food processing, is often regarded as an evolutionary key innovation that has played an important role in their trophic diversification (Liem 1973). However, recent phylogenetic analyses suggest that the accelerated rate of diversification in East African cichlids occurred within the last 2.4 Myr, well after the acquisition of the PJA (Seehausen 2006; Salzburger 2009). This significant time lag has led several authors to suggest that the high speciation rates in many labrid and cichlid clades are better correlated with the evolution of sexual characters (Alfaro et al. 2009; Salzburger 2009), suggesting a predominant role of sexual selection in these diversifications. Interestingly, the ecologically important and plastic PJA has also allowed the evolution of mouth-brooding behaviour and the production of species-specific courtship sounds in male cichlids (Amorim et al. 2004), which have the potential to promote enhanced behavioural isolation. It is likely that this important evolutionary innovation might have served a twofold role: a historical role in trophic adaptation and a more recent (derived) role in sexual selection. Clearly, the role of the PJA in the radiation of cichlids remains open to investigation (Danley & Kocher 2001; Schön & Martens 2004; Alfaro et al. 2009). More generally, the interplay among shared ecological contexts, shared life history attributes and unique one-off innovations in promoting diversification and parallelism remains an intriguing area of ongoing research.