Recurrent changes in cichlid dentition linked to climate‐driven lake‐level fluctuations

Abstract

Climate‐induced habitat change has often been invoked as an important driver of speciation and evolutionary radiation in cichlid fishes, yet studies linking morphological change directly to long‐term environmental fluctuations are scarce. Here, we track changes through time in the oral dentition of Oreochromis hunteri, the endemic and only indigenous fish species inhabiting the East African crater Lake Chala (Kenya/Tanzania), in relation to climate‐driven lake‐level fluctuations during the last 25,000 yr. Fossil teeth were recovered from six periods representing alternating high and low lake‐level stands associated with late‐Pleistocene and Holocene trends in rainfall and drought. To construct a reference framework for morphological variation in fossil assemblages, we first analyzed the variability in oral tooth morphology within the modern‐day fish population. These analyses established that, like other cichlids, O. hunteri gradually replace their bicuspid/tricuspid oral dentition with more unicuspid teeth as they grow. In the fossil assemblages, we found systematic and recurrent changes in the relative abundance of these oral tooth types, with a higher proportion of unicuspids during low‐stands. Moreover, O. hunteri living during low‐stands systematically developed unicuspid dentition at a smaller body size, compared with conspecifics living during high‐stands. Considering that low‐stand conditions created a sizable area of oxygenated soft‐bottom habitat that is lacking during high‐stands, we propose that the associated change in oral dentition reflects the fishes’ exploitation of this new habitat either for feeding or for reproduction. The recurrent nature of the observed shifts provides evidence for the ability of O. hunteri to systematically adapt to local habitat change, and strongly suggests that morphological change in oral dentition promoted its long‐term population persistence in an aquatic ecosystem presenting the dual challenge of being both sensitive to climate change (creating constantly shifting selective pressures) and isolated from surrounding populations (limiting gene flow). In Lake Chala, ancient climate‐driven lake‐level fluctuations did not directly promote speciation in O. hunteri, but the population bottlenecks they may have caused potentially contributed to its divergence from sister species Oreochromis jipe.

Astatotilapia species (Teleostei, Cichlidae) from Malawi, Mozambique and Tanzania, excluding the basin of Lake Victoria.

“…The closest relationship was with haplochromines from Lake Chala, which the authors interpret as indicative of a former natural connection between the two water bodies. However, subsequent authors have suggested that the haplochromines in Chala are not native (Moser et al 2018;Dieleman et al 2019). We would identify all these as representing the 'sparsidens' lineage of Astatotilapia bloyeti, which is consistent with the illustration of a freshly collected male from Ngare Nanyuki.…”

An integrative paleolimnological approach for studying evolutionary processes

“…Recovering fish macroremains (e.g. teeth) from sediment cores can help track morphological evolution of ecologically relevant traits [14] and past patterns of fish community composition [15]. Applying these methods within a broader paleolimnological approach could help us understand both microevolutionary dynamics of populations (e.g.…”

“…Often, selective environments are influenced by multiple interacting biotic and abiotic factors and the link between organismal phenotype and fitness is both complex and environmentally contingent [35]. Integrating paleolimnological evidence with geological records of phenotypic variation allows us to examine how changing ecological conditions drive morphological variation in key taxa and test hypotheses about past selective environments [5,14]. The continuous archives of phenotypic data preserved in lake sediments spanning from annual to millennial timescales provide unique and complementary insights into the temporal dynamics of phenotypic evolution.…”

“…For example, a previous study has linked the rate of trait diversification within a gastropod radiation with long-term changes in climate and lake-level fluctuations [48]. A similar approach applied to other taxa that preserve morphological remains in lake sediments could also be used to track the progression of adaptive radiations [14]. In addition to morphological evidence from macroremains, recovering genetic material from sediments and fossils (Box 2) might provide an additional source of inference about the underlying drivers of variation in diversification rates among and within lineages.…”

Ancient DNA is preserved in fish fossils from tropical lake sediments

“…In many of these study systems, such as Darwin's finches, Heliconius butterflies, Hawaiian silverswords or Anolis lizards, a challenge for palaeogenetics is the scarcity of well-preserved fossil remains. An exception to this general paucity of fossils from geologically young and extant radiations are the cichlid fishes of East Africa, which can leave chronologically highly resolved records of bones, bone fragments, teeth and scales in the sediments of lakes (Ngoepe et al, 2023;Cohen et al, 2016;Dieleman et al, 2015Dieleman et al, , 2019Muschick et al, 2018;Reinthal et al, 2010). Yet, whether such remains contain appreciable amounts of endogenous aDNA is unknown.…”