Parallel genetic basis for repeated evolution of armor loss in Alaskan threespine stickleback populations

Abstract

Most adaptation is thought to occur through the fixation of numerous alleles at many different loci. Consequently, the independent evolution of similar phenotypes is predicted to occur through different genetic mechanisms. The genetic basis of adaptation is still largely unknown, however, and it is unclear whether adaptation to new environments utilizes ubiquitous small-effect polygenic variation or large-effect alleles at a small number of loci. To address this question, we examined the genetic basis of bony armor loss in three freshwater populations of Alaskan threespine stickleback, Gasterosteus aculeatus, that evolved from fully armored anadromous populations in the last 14,000 years. Crosses between complete-armor and low-armor populations revealed that a single Mendelian factor governed the formation of all but the most anterior lateral plates, and another independently segregating factor largely determined pelvic armor. Genetic mapping localized the Mendelian genes to different chromosomal regions, and crosses among these same three widely separated populations showed that both bony plates and pelvic armor failed to fully complement, implicating the same Mendelian armor reduction genes. Thus, rapid and repeated armor loss in Alaskan stickleback populations appears to be occurring through the fixation of large-effect variants in the same genes.

Fig. 1.

Map of the Matanuska-Susitna (Mat-Su) Valley of Alaska with trypsin clearedandAlizarinredstainedsticklebackshowingBootLake(A),BearPawLake(B) and Whale Lake (C) freshwater low-armor populations, and anadromous Rabbit Slough complete-armor ancestor (D). The complete-armor anadromous form has a full set of lateral plates and fully formed pelvic structure (arrows), whereas each freshwater population lacks most of the lateral plates and has either highly reduced (Boot, Bear Paw) or completely absent (Whale) pelvic structures. Blue dots indicate additional populations with mostly complete pelvic structure (mean score of 5.0), red are mostly intermediate (2.0–4.0), and yellow are low (0.0–2.0).

Fig. 2.

Distribution of number of lateral plate and pelvic structure scores in wild-caught complete-armor anadromous (A and B, Wild Anadromous), laboratory-bred and reared anadromous (C and D, Lab Anadromous), low-armor freshwater parental populations (E and F, Wild Lacustrine; ∼100 individuals each pooled from Bear Paw, Boot, and Whale Lakes), lab-reared fish from intrapopulation low-armor crosses (G and H, Lab Lacustrine; pool of ∼100 individuals from each population), F₁ complementation hybrid (I and J, Complementation; pool of offspring from Bear Paw-by-Boot and Boot-by-Whale crosses), F₁ mapping hybrids (K and L, F₁ Mapping; pool of all F₁ fish from crosses between anadromous-by-each low-armor population), and F₂ mapping hybrid (M and N,F₂ Mapping; pool of F₂ fish from full-sib crosses of F₁ Mapping individuals from anadromous-by-each low-armor parent). The lateral plate number and pelvic scores are the average of the left and right sides of the fish. Numbers above data in the F₂ Mapping panels (M and N) are the counts of the complete to low lateral plate and pelvic structure classes respectively, indicating an approximate 3:1 ratio for each trait.

Fig. 3.

Comparison of the mean (SE) pelvic scores across intrapopulation (Non-Hybrid) crosses of bear paw (BP), boot (B), and whale (W), low-by-low complementation (L × L Hybrid) crosses of Bear Paw-by-Boot (BP × B) and Boot-by-Whale (B × W), and the low-pelvic class of the low-by-anadromous F₂ hybrids (L × A F₂ Hybrid) whose parents were the product of Bear Paw-by-Anadromous (BP × A), Boot-by-Anadromous (BP × A), and Whale-by-Anadromous (BP × A) crosses. Only individuals from the low-pelvic class (scores < 5) were used to calculate the statistics for the L × AF₂ hybrid families presented here.

Fig. 4.

Representative phenotypes of the parental complete armor (A), parental low armor (B), F₁ mapping hybrid (C), and F₂ mapping hybrid (D–G) generations. The major axes of variation in the F₂ intercross generation indicate the segregation of armor loss as a 9:3:3:1 dihybrid Mendelian ratio (red; observed ratio in black) of the parental armor classes. (D) The complete-armor phenotype of the F₂ generation. (G) The low-armor phenotype. (E and F) The complete-plate/low-pelvic structure and complete-pelvic/low-plate recombinant phenotypes, respectively.

Fig. 5.

Positions of Alaskan Mendelian lateral plate (Mendelian Lateral Plate Locus) and pelvic (Mendelian Pelvic Locus) loci on the stickleback linkage map (22). Alaskan Mendelian plate and pelvic loci localized to linkage group (LG) VII and LGXVIII, respectively. The Alaskan lateral plate locus maps 1.1 centi-Morgans (cM) away from Stn183, and the pelvic phenotype locus maps 7.3 cM from marker Stn82. Open boxes on the right side of the figure indicate the position of QTLs important for lateral plate and pelvic spine variation in a cross between low-plate, complete-pelvic stickleback species from British Columbia (22).