The frequent occurrence of adaptive radiations on oceanic islands and in lakes is often attributed to ecological opportunity resulting from release from competition where arrival order among lineages predicts which lineage radiates. This occurs when the lineage that arrives first expands its niche breadth and diversifies into a set of ecological specialists with associated monopolization of the resources. Later-arriving species do not experience ecological opportunity and do not radiate. While theoretical support and evidence from microbial experiments for priority effects are strong, empirical evidence in nature is difficult to obtain. Lake Victoria (LV) is home to an exceptional adaptive radiation of haplochromine cichlid fishes, where 20 trophic guilds and several hundred species emerged in just 15 000 years, the age of the modern lake that was preceded by a complete desiccation lasting several thousand years. However, while about 50 other lineages of teleost fish also have established populations in the lake, none of them has produced more than two species and most of them did not speciate at all. Here, we test if the ancestors of the haplochromine radiation indeed arrived prior to the most competent potential competitors, 'tilapias' and cyprinids, both of which have made rapid radiations in other African lakes. We assess LV sediment core intervals from just before the desiccation and just after refilling for the presence of fossil fish teeth. We show that all three lineages were present when modern LV began to fill with water. We conclude that the haplochromines' extraordinary radiation unfolded in the presence of potentially competing lineages and cannot be attributed to a simple priority effect.
Tropical freshwater lakes are well-known for their high biodiversity, and the East African Great Lakes in particular are renowned for their endemic cichlid fish adaptive radiations. While comparative phylogenetic analyses of extant species flocks have revealed patterns and processes of their diversification, evolutionary trajectories within lineages, impacts of environmental drivers, or the scope and nature of now-extinct diversity remain largely unknown. Time-structured paleodata from geologically young fossil records, such as fossil counts and particularly ancient DNA data, would help fill this large knowledge gap. High ambient temperatures can be detrimental to the preservation of DNA, but refined methodology now allows data generation even from very poorly preserved samples. Here, we show for the first time that fish fossils from tropical lake sediments yield endogenous ancient DNA (aDNA). Despite generally low endogenous content and high sample drop-out, high-throughput sequencing and in some cases sequence capture allowed for taxonomic assignment to family or tribe level and phylogenetic placement of individuals. Even skeletal remains weighing less than 1 mg and up to 2700 years of age could be phylogenetically placed. We find that the relationship of degradation of aDNA with the thermal age of samples is similar to that described for terrestrial samples from cold environments adjusted for elevated temperatures. Success rates and aDNA preservation differed between the investigated lakes Chala, Kivu and Victoria, possibly caused by differences in water oxygenation at deposition. Our study demonstrates that sediments of tropical lakes preserve genetic information on rapidly diversifying taxa over time scales of millennia.
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