Origin of the Laurentian Great Lakes fish fauna through upward adaptive radiation cascade prior to the Last Glacial Maximum

Abstract

The evolutionary histories of adaptive radiations can be marked by dramatic demographic fluctuations. However, the demographic histories of ecologically-linked co-diversifying lineages remain understudied. The Laurentian Great Lakes provide a unique system of two such radiations that are dispersed across depth gradients with a predator-prey relationship. We show that the North American Coregonus species complex ("ciscoes") radiated rapidly prior to the Last Glacial Maximum (80-90 kya), a globally warm period, followed by rapid expansion in population size. Similar patterns of demographic expansion were observed in the predator species, Lake Charr (Salvelinus namaycush), following a brief time lag, which we hypothesize was driven by predator-prey dynamics. Diversification of prey into deep water created ecological opportunities for the predators, facilitating their demographic expansion, which is consistent with an upward adaptive radiation cascade. This study provides a new timeline and environmental context for the origin of the Laurentian Great Lakes fish fauna, and firmly establishes this system as drivers of ecological diversification and rapid speciation through cyclical glaciation.

Fig. 1. Ecological variation and population structure in Great Lakes salmonids.

a Depth profile of Lake Superior showing bathymetric distributions of Coregonus artedi, C. hoyi, C. kiyi, and two morphs of Salvelinus namaycush (lean and siscowet). Artwork provided by Joseph R. Tomelleri. b Maximum likelihood phylogenetic tree with branch support calculated through 1,000 ultrafast bootstrap replicates. PCA of genetic variation in (c) C. artedi, C. hoyi, C. kiyi, C. nigripinnis and (d) S. namaycush lean and siscowet derived from single nucleotide polymorphisms with no missing data. Source data are available at 10.5061/dryad.n02v6wx59.

Fig. 2. Environmental context of diversification and historical demography of Great Lakes salmonids.

a Mean surface-air temperature of the continental Northern Hemisphere through time, relative to present day. Temperature data from De Boer, Lourens, and Van De Wal. b Estimates of effective population size through time via PSMC analysis for four species of Coregonus (C. artedi, C. hoyi, C. kiyi, C. nigripinnis) and Salvelinus namaycush (lean and siscowet). Dark grey bar indicates the time range of the Last Glacial Maximum (19–33 kya). Light grey bars indicate time points (10.5, 13, 15.5, 17.5 kya) of deglaciation stages (c) of the Laurentian Great Lakes basin. Shapefiles for glacial margins as well as river and lake boundaries obtained from Dalton et al. and https://www.naturalearthdata.com respectively. Source data are available at 10.5061/dryad.n02v6wx59.