Impacts of Quaternary Climatic Changes on the Diversification of Riverine Cichlids in the Lower Congo River

Climatic and geomorphological changes during the Quaternary period impacted global patterns of speciation and diversification across a wide range of taxa, but few studies have examined these effects on African riverine fish. The lower Congo River is an excellent natural laboratory for understanding complex speciation and population diversification processes, as it is hydrologically extremely dynamic and recognized as a continental hotspot of diversity harboring many narrowly endemic species. A previous study using genome-wide SNP data highlighted the importance of dynamic hydrological regimes to the diversification and speciation in lower Congo River cichlids. However, historical climate and hydrological changes (e.g., reduced river discharge during extended dry periods) have likely also influenced ichthyofaunal diversification processes in this system. The lower Congo River offers a unique opportunity to study climate-driven changes in river discharge, given the massive volume of water from the entire Congo basin flowing through this short stretch of the river. Here, we, for the first time, investigate the impacts of paleoclimatic factors on ichthyofaunal diversification in this system by inferring divergence times and modeling patterns of gene flow in four endemic lamprologine cichlids, including the blind cichlid, Lamprologus lethops. Our results suggest that Quaternary climate changes associated with river discharge fluctuations may have impacted the diversification of species along the system and the emergence of cryptophthalmic phenotype in some endemic species. Our study, using reduced representation sequencing (2RADseq), indicates that the lower Congo River lamprologines emerged during the Early-Middle Pleistocene transition, characterized as one of the earth's major climatic transformation periods. Modeling results suggest that gene flow across populations and between species was not constant but occurred in temporally constrained pulses. We show that these results correlate with glacial-interglacial fluctuations. The current hyper-diverse fish assemblages of the lower Congo River riverscape likely reflect the synergistic effects of multiple drivers fueling complex evolutionary processes through time.