Evolution and diversity of two cisco forms in an outlet of glacial Lake Algonquin

Abstract

The diversity of Laurentian Great Lakes ciscoes (Coregonus artedi, sensu lato) arose via repeated local adaptive divergence including deepwater ciscoes that are now extirpated or threatened. The nigripinnis form, or Blackfin Cisco, is extirpated from the Great Lakes and remains only in Lake Nipigon. Putative nigripinnis populations were recently discovered in sympatry with artedi in a historical drainage system of glacial Lake Algonquin, the precursor of lakes Michigan and Huron. Given the apparent convergence on Great Lakes form, we labeled this form blackfin. Here, we test the hypothesis that nigripinnis may have colonized this area from the Great Lakes as a distinct lineage. It would then represent a relict occurrence of the historical diversity of Great Lakes ciscoes. Alternatively, blackfin could have evolved in situ in several lakes. We captured more than 600 individuals in the benthic or pelagic habitat in 14 lakes in or near Algonquin Provincial Park (Ontario, Canada). Fish were compared based on habitat, morphology, and genetic variation at 6,676 SNPs. Contrary to our expectations, both cisco and blackfin belonged to an Atlantic lineage that colonized the area from the east, not from the Great Lakes. Sympatric cisco and blackfin were closely related while fish from different lakes were genetically differentiated, strongly suggesting the repeated in situ origin of each form. Across lakes, there was a continuum of ecological, morphological, and genetic differentiation that could be associated with alternative resources and lake characteristics. This study uncovers a new component of cisco diversity in inland lakes of Canada that evolved independently from ciscoes of the Laurentian Great lakes. The diversity of cisco revealed in this study and across their Canadian range presents a challenge for designating conservation units at the intraspecific level within the framework of the Committee on the Status of Endangered Wildlife in Canada (COSEWIC).

Keywords: Mysis diluviana; adaptive radiation; blackfin; cisco; nigripinnis; postglacial recolonization.

Figure 1

(a) Location of Algonquin Provincial Park (in green) and reference lakes outside the focal area (outlined by dotted lines) detailed in (b). Artedi are shown in gray and nigripinnis in black. In blue is the approximate area covered by proglacial L. Algonquin and Champlain Sea at 12 500 cal. BP. adapted from Dyke (2004). (b) Location of the focal area. Benthic and pelagic ciscoes are respectively colored in black and gray. For lakes with only cisco, code names as per Table 1 are provided. For lakes with sympatric forms of ciscoes, full names are provided in bold. Red arrow is the head of the Fossmill outlet

Figure 2

Landmarks used to characterize morphological diversity of ciscoes in Algonquin Provincial Park. (1) Anterior tip of the snout, (2) midpoint of hypural plate, (3) anterior tip of eye, (4) posterior tip of eye, (5) center of eye, (6) top of cranium at middle point of eye, (7) posterior of neurocranium, (8) anterior insertion of dorsal fin, (9) posterior insertion of dorsal fin, (10) anterior insertion of adipose fin, (11) dorsal insertion of caudal fin, (12) ventral insertion of caudal fin, (13) posterior insertion of anal fin, (14) anterior insertion of anal fin, (15) tip of anal fin, (16) insertion point of pelvic fin, (17) tip of pelvic fin, (18) insertion point of pectoral fin, (19) tip of pectoral fin, (20) isthmus of branchiostegal membrane, (21) posterior tip of maxilla, (22) posterior tip of opercular, (23–24) calibration landmarks. Interorbital width was also measured directly on fish with a digital millimeter caliper (not shown)

Figure 3

Gill‐raker counts of ciscoes sampled in Algonquin Provincial Park, L. Memesagamesing, and L. Nipigon. Fish caught in benthic and pelagic nets are respectively colored in black and gray. Lakes with Mysis with only pelagic ciscoes are pooled (2 lakes, 60 individuals) because they had very similar gill‐raker counts. The same was done for lakes without Mysis harboring only pelagic ciscoes (5 lakes, 154 individuals). Fishes from L. Nipigon were visually assigned to nigripinnis or artedi by T. Pratt and are respectively colored in black and gray

Figure 4

Comparison of phenotypes between sympatric forms based on habitat of capture (BEN or PEL) for (a) gill rakers, (b) linear traits, and (c) shape. Symbols are for L. Cedar (✳), L. Hogan (), L. Cauchon (), L. Memesagamesing (), L. Mink (), L. Radiant (), and L. Nipigon (, absent in shape analyses). Lakes with only pelagic cisco (L. Dickson, L. Craig, L. Catfish, L. Three Mile, L. Carl Wilson, L. Big Crow, and L. Grand) are illustrated by a cross (+), and L. Kioshkokwi with only benthic cisco is in gray. For illustrative purposes, dotted lines join BEN and PEL ecotypes from the same lake

Figure 5

Bar plot output from ADMIXTURE illustrating ancestry (q‐value) for preferred number of groups (K). Lake codes are as per Table 1; BEN: benthic; PEL: pelagic. (a) Genetic clusters with focal and reference lakes at K = 2. (b) Genetic clusters in Algonquin Provincial Park and L. Memesagamesing at K = 7

Figure 6

(Re)classification success in L. Cedar and L. Hogan when ciscoes are grouped by habitat of capture (BEN or PEL) in white versus gill‐raker counts (LGR or HGR) in black. Symbols □/■ are for genetic data, △/▲ are for shape data, and ○/● are for linear morphometrics