Arrival order and release from competition does not explain why haplochromine cichlids radiated in Lake Victoria

Abstract

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.

The Paradox Behind the Pattern of Rapid Adaptive Radiation: How Can the Speciation Process Sustain Itself Through an Early Burst?

“…There is no question that ecological opportunity is associated with adaptive radiation and diversification at global and regional scales; indeed, this remains the dominant explanation within the ecological theory of adaptive radiation. However, on closer inspection of some taxa at microevolutionary scales, key innovations do not always coincide with increased diversification (Alfaro et al 2009a, Harmon & Harrison 2015, McGee et al 2015, Rabosky 2017, Seehausen 2006), many taxa colonize new environments and fail to diversify (Arbogast et al 2006, Lovette et al 2002, Martin 2016a, Martin & Wainwright 2013a, Meyer et al 2017, Muschick et al 2018, Roderick & Gillespie 1998, and diversification of new lineages often precedes or lags long after mass extinction events (reviewed in Erwin 2015). Furthermore, niche axes relevant to ecological opportunity and diversification are rarely tested a priori (e.g., Schluter & Grant 1984a;reviewed in Erwin 2015, Stroud & Losos 2016, Wellborn & Langerhans 2015.…”

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

“…, Muschick et al. ), diverse methodological and confounding factors have thus far prevented detailed study of environment–phenotype relations in individual cichlid species lineages (Dieleman et al. ).…”

“…Cichlid teeth and scales preserved in the sediments of existing African lakes hold the best hope for a continuous record (Cohen 2012). Although such records are now tentatively being explored (Reinthal et al 2011, Muschick et al 2018, diverse methodological and confounding factors have thus far prevented detailed study of environment-phenotype relations in individual cichlid species lineages (Dieleman et al 2015).…”

Detecting the macroevolutionary signal of species interactions

“…For example, anole lizards on Greater Antillean islands show speciation rates that decline as species richness increases on each island (Rabosky & Glor, 2010). Alternatively, the order of arrival to a geographic region (Tanentzap et al, 2015) and the properties of competing lineages that arrive concurrently (Muschick et al, 2018;Wagner, Harmon, & Seehausen, 2014) might predict diversification rate. The fossil record, alone or in conjunction with phylogenetic trees, can also provide substantial insights into the diversity dynamics in evolving clades (Pires, Silvestro, & Quental, 2017;Quental & Marshall, 2010).…”

“…Ultimately, expanding our use of mechanistic models as tools embedded in a diverse, interdisciplinary toolkit will enrich our ability to be effective evolutionary detectives (Losos, ). We cannot travel back in time to collect data on distant macroevolutionary events (Muschick et al., ), but biologically informed and clearly defined models linking species interactions to macroevolutionary changes will aid us in our ability to rigorously evaluate whether macroevolutionary patterns are consistent with species interaction hypotheses.…”