Evol Ecol Res 15: 413-435 (2013)     Full PDF if your library subscribes.

Regressive evolution of the pelvic complex in stickleback fishes: a study of convergent evolution

Tom Klepaker1, Kjartan Østbye2,3 and Michael A. Bell4

1Department of Biology, Aquatic Behavioural Ecology Research Group, University of Bergen, Bergen, Norway,  2Department of Biology, Centre for Ecological and Evolutionary Synthesis (CEES), University of Oslo, Oslo, Norway,  3Department of Forestry and Wildlife Management, Hedmark University College, Elverum, Norway and  4Department of Ecology and Evolution, Stony Brook University, Stony Brook, New York, USA

Correspondence: T. Klepaker, Department of Biology, Aquatic Behavioural Ecology Research Group, University of Bergen, PO Box 7800, N-5020 Bergen, Norway.
e-mail: tom.klepaker@bio.uib.no


Background: Regressive evolution of the pelvic complex has been observed in populations of three of five stickleback genera, Gasterosteus, Pungitius, and Culaea, from young freshwater habitats (<18,000 years old). It has been hypothesized to be selected for by ion limitation, lack of predation by fishes, and increased predation by large aquatic insects. Stickleback pelvic reduction is often caused by deletion mutations of the Pitx1 gene, which prevent its expression during pelvic development. Lack of Pitx1 expression may be partly compensated for by Pitx2, which is preferentially expressed on the left side of the body, causing the left pelvic vestige to be larger than the right. Thus, left-biased directional asymmetry of pelvic vestiges implicates null Pitx1 alleles.

Aim: Review the geographical patterns of pelvic variation in the three stickleback genera and consider their implications for hypotheses regarding the genetics and evolution of pelvic reduction in the Gasterosteidae.

Data: We review published data on pelvic reduction and add previously unpublished information from populations in Scotland and Norway.

Methods: We assign individual stickleback to one of three pelvic phenotypes – normal, vestigial, and lost pelvis – and explore the distribution of these three broad classes among populations. We study bilateral symmetry of the pelvis by scoring pelvic phenotypes on the left and right sides.

Results: Pelvic reduction is rare in sticklebacks and occurs only in fresh water. Sticklebacks with pelvic reduction tend to occur in the western and northern parts of their ranges in Eurasia and North America, but this pattern is less evident for the ninespine stickleback. Pelvic phenotype frequency distributions within populations differ among stickleback genera. The vestigial pelvic phenotype dominates in many populations of Gasterosteus aculeatus, rarely in Pungitius, and never in Culaea inconstans. In Culaea, the lost and normal pelvic phenotypes are often dimorphic, but a vestigial pelvis is rare. This dimorphism does not occur in the other two genera. Monomorphism of the lost pelvic phenotype does not occur in Gasterosteus, and is rare in the other two genera. Asymmetry of pelvic vestiges is common in all three genera, but left-larger directional asymmetry predominates only in Gasterosteus. This bias could be due to the suggested regulatory mutation in the Pitx1 gene and/or mutations in downstream targets of Pitx1, and suggests involvement of other genes for pelvic reduction in the other genera.

Keywords: convergent evolution, directional asymmetry, Gasterosteidae, pelvic reduction, regressive evolution, stickleback.

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