Illuminating the Drivers of Genomic Diversification in Lamprologine Cichlids of the Lower Congo River
Date of Degree
Michael J. Hickerson
S. Elizabeth Alter
Melanie L. J. Stiassny
Ana Carolina Carnaval
Biodiversity | Bioinformatics | Biology | Genomics
fish, gene flow, freshwater, population genomics, climate change, evolution
Freshwater fishes are extraordinarily diverse, considering their available habitats represent a tiny proportion of the earth’s surface. Rivers connect heterogeneous habitats in a linear form and provide excellent simplified models to understand how aquatic biodiversity evolves. In particular, the lower Congo River (LCR) in west Central Africa consists of a dynamic hydroscape exhibiting extraordinary aquatic biodiversity, endemicity, and morphological and ecological specialization. This system is thus an excellent natural laboratory for understanding complex speciation and population diversification processes. In my research, I explore various drivers of diversification, and adaptive evolution in rheophilic lamprologine cichlids endemic to the LCR, including Lamprologus lethops, the only blind cichlid fish are known to exist.
I first focus on understanding the evolutionary relationships between four endemic lamprologine cichlid species distributed along the mainstream of the LCR without habitat range overlap, as well as spatially explicit population structure within each species. I also investigate how allopatric speciation plays a role in the diversification and infer gene flow rates and flow direction using genome-wide SNP data. Previous studies suggest that numerous high-energy rapids present in the LCR are physical barriers to gene flow, thus facilitating diversification and generating ichthyofaunal diversity. This study suggests high-energy rapids serve as physical barriers to gene flow that generate genetic divergence at interspecific and intraspecific levels but may also provide multidirectional dispersal opportunities for riverine cichlid fishes instead of simply downstream directionality. This study was published in Molecular Ecology in May 2022.
To further understand the drivers of speciation in this system, I explore the impact of extrinsic forces, such as paleoclimate changes, on the timing of diversification and gene flow patterns across these species. The Quaternary’s climatic changes significantly impacted global patterns of speciation across various terrestrial taxa; however, few studies have examined these effects in African freshwater fishes. I infer demographic history and model different historical gene flow scenarios to understand how the Quaternary glacial-interglacial fluctuations might have impacted the riverine cichlids. My study reveals that riverine LCR lamprologine species emerged during the Early-Middle Pleistocene transition, known as one of the earth’s major climatic transformation periods. Model selection results of different historical gene flow scenarios suggest some environmental changes (e.g., during the warmer interglacial period) might have influenced the consistency of gene flow. Additionally, the estimated timing of divergence is correlated with glacial-interglacial fluctuations, particularly with the reduction in river discharge during extended dry periods. Interestingly, the adaptation of the precursor species of the cryptophthalmic L. lethops to a deep water environment might have been initiated during significantly reduced river discharges due to an extensive dry period.
Finally, I examine how troglomorphism emerged in Lamprologus lethops. The LCR displays extraordinary examples of convergent evolution where many fishes, from families across the tree of life, exhibit features similar to those found in cavefishes, known as troglomorphic and/or cryptophthalmic phenotypes. The processes of degenerative evolution, including eye reduction, loss of image formation, and loss of skin pigmentation, are not clearly understood. I investigate whether previously suggested loss-of-function mutations are present across five additional whole genomes of the cryptophthalmic L. lethops, and also look for signatures of hard selective sweeps. I additionally look for signatures of concerted population bottlenecks by investigating effective population size changes in populations of L. lethops and its LCR congener, L. tigripictilis, from different geographical regions. The study suggests that the degenerative evolution of L. lethops might have occurred through the relaxation of purifying selection (i.e., relaxation in the elimination of deleterious mutations, including inactivation mutations) accompanied by neutral processes, such as genetic drift. Since genetic drift can increase the frequency of inactivating mutations when population size is reduced, a severe population reduction (i.e., population bottleneck) as inferred in my study might have caused more rapid drift, which may in turn aid loss-of-function mutations to increase in frequency. Furthermore, I observe an agreement in patterns between the concerted reduction of population sizes (i.e., bottleneck) of two congener species from different geographical regions and the cooling of the earth’s climate (e.g., the Last Glacial Maximum). I suggest that paleoclimate changes might have significantly impacted the evolutionary processes of riverine cichlids, including the cryptophthalmic L. lethops.
Kurata, Naoko P., "Illuminating the Drivers of Genomic Diversification in Lamprologine Cichlids of the Lower Congo River" (2023). CUNY Academic Works.