Abstract

Factors ranging from ecological opportunity to genome composition might explain why only some lineages form adaptive radiations. While being rare, particular systems can provide natural experiments within an identical ecological setting where species numbers and phenotypic divergence in two closely related lineages are notably different. We investigated one such natural experiment using two de novo assembled and 40 resequenced genomes and asked why two closely related Neotropical cichlid fish lineages, the Amphilophus citrinellus species complex (Midas cichlids; radiating) and Archocentrus centrarchus (Flyer cichlid; nonradiating), have resulted in such disparate evolutionary outcomes. Although both lineages inhabit many of the same Nicaraguan lakes, whole‐genome inferred demography suggests that priority effects are not likely to be the cause of the dissimilarities. Also, genome‐wide levels of selection, transposable element dynamics, gene family expansion, major chromosomal rearrangements and the number of genes under positive selection were not markedly different between the two lineages. To more finely investigate particular subsets of the genome that have undergone adaptive divergence in Midas cichlids, we also examined if there was evidence for ‘molecular pre‐adaptation’ in regions identified by QTL mapping of repeatedly diverging adaptive traits. Although most of our analyses failed to pinpoint substantial genomic differences, we did identify functional categories containing many genes under positive selection that provide candidates for future studies on the propensity of Midas cichlids to radiate. Our results point to a disproportionate role of local, rather than genome‐wide factors underlying the propensity for these cichlid fishes to adaptively radiate.

Highlights

  • Some lineages of organisms phenotypically diversify and rapidly speciate to form adaptive radiations

  • The inferred earlier colonization of crater Lake Xiloá by Ar. centrarchus argues against a role for priority effects in promoting diversification in Midas cichlids (Figure 1). This result is consistent with previous work on Midas cichlids and Ar. centrarchus based on lower-resolution genetic data (Franchini et al, 2017; Fruciano, Franchini, Kovacova, et al, 2016; Fruciano, Franchini, Raffini, et al, 2016)

  • Our further examination of demographics reveals a second wave of colonization for both species, which is consistent with previous analysis in Ar. centrarchus (Franchini et al, 2017)

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Summary

| INTRODUCTION

Some lineages of organisms phenotypically diversify and rapidly speciate to form adaptive radiations. There is no evidence that any of these other lineages have speciated within this system (Elmer et al, 2013; Franchini et al, 2017; Fruciano et al, 2016) and they show little phenotypic divergence (Fruciano, Franchini, Kovacova, et al, 2016; Fruciano, Franchini, Raffini, et al, 2016) These closely related cichlid lineages, such as the flyer cichlid Ar. centrarchus that shared a last common ancestor only a few million years ago with the Midas cichlid lineages (Hulsey et al, 2010), provide ideal candidates for comparisons with Midas cichlids since they live in the same habitats including the older large Lakes Nicaragua and Managua as well as several of the much younger crater lakes. These analyses provide an integrative and comparative examination of the genomic conditions underlying the Midas cichlid adaptive radiation

| METHODS
| RESULTS
Findings
| DISCUSSION

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