The Functional Basis of Natural Selection for Vertebral Traits of Larvae in the Stickleback Gasterosteus aculeatus

Abstract

Previous studies have demonstrated selective predation for vertebral traits of larvae in the stickleback Gasterosteus aculeatus. I tested the hypothesis that this selection results from a direct functional advantage to particular vertebral phenotypes by direct measurement of the burst swimming performance of larvae. Within a narrow window of lengths, burst speed did depend on vertebral phenotype. As in the previous predation experiments, performance was related more directly to the ratio of abdominal to caudal vertebrae (VR) than to the total number of vertebrae (VN), and the optimal VR decreased as larval length increased. Changes with length in the vertebral phenotype frequencies of wild larvae provided evidence of selection for VR and for VN in the wild. Larvae with particular VR increased in frequency in the wild at just those lengths when their relative performance was superior in the laboratory. The observed pattern of length-dependent selection for vertebral number provides an explanation for the widespread trends in vertebral number that occur among populations of related fishes.

Genetic Architecture of Skeletal Evolution in European Lake and Stream Stickleback

“…The source populations of the cross showed clear divergence in the number of vertebrae, with a higher average count in lake than stream fish. This trend has also been found in other studies comparing lake and stream stickleback (Hagen and Gilbertson 1972;Reimchen et al 1985) and thus likely represents an adaptive response to divergent selection on locomotion (Swain 1992). Although further functional evidence is needed, our finding that vertebral number is genetically unrelated to body size (as also found in a different stickleback system; Alho et al 2011) indicates that population divergence in the number of vertebrae is unlikely to reflect a correlated response to selection on size (note that the ROM lake and CHE stream populations differ in size; Moser et al 2012).…”

“…Stickleback populations often differ in the number of vertebrae (Hagen and Gilbertson 1972;Moodie and Reimchen 1976;Reimchen et al 1985). Although the functional basis of this variation remains poorly understood (but see Swain 1992), genetic analysis in stickleback may provide insights into vertebral diversification in other fish (Ward and Brainerd 2007;McDowall 2008) and vertebrates in general. As a first step, we thus produced whole-body X-ray scans of 14 specimens from each natural source population, counted all vertebrae excluding the urostyle (Fig.…”

A Quantitative Genetic Test of Adaptive Decoupling Across Metamorphosis for Locomotor and Life-History Traits in the Pacific Tree Frog, Hyla Regilla

“…Maximum locomotor performance (i.e., burst speed, sustained speed, endurance) has been studied in many natural populations and possesses the basic attributes for potential adaptive evolution (Bennett and Huey 1990). Interindividual variation in locomotor performance is temporally repeatable (see table 1 of Austin and Shaffer 1992), is subject to selection in some populations (Jayne and Bennett 1990;Swain 1992;Watkins 1996), and often has some heritable genetic component (Garland 1988;Tsuji et al 1989;Sorci et al 1995;Dohm et al 1996). On the basis of these findings, Carrier (1996) proposed that adult locomotor performance often evolves primarily in response to selection on juveniles, a hypothesis that requires a genetic correlation between juvenile and adult performance.…”

Can spatial sorting associated with spawning migration explain evolution of body size and vertebral number inAnguillaeels?

“…For instance, it has been proposed that body elongation and VN are related to feeding performance, such as rotational feeding and knotting behavior used by these gape-limited predators to tear large prey into smaller ingestible pieces (Mehta et al, 2010). Previous studies also report on associations of VN with neonate body size (Arnold & Bennett, 1988;Harding, 1985;Lindell et al, 1993), juvenile growth rate (Swain, 1992a;Tibblin et al, 2016), survival (Lindell et al, 1993;Swain, 1992b;Tibblin et al, 2016), and female reproductive investment (Tibblin et al, 2016). In addition, the distribution of VN may be affected by stabilizing selection operating within populations, as recently reported for pike (Tibblin et al, 2016).…”

“…Previous studies suggest that larger body size is linked to increased locomotion, endurance, and a higher capacity for long-distance dispersal in various organisms (Forsman, 1996;Forsman et al, 2011;Foster, 1964;Hemptinne, Magro, Evans, & Dixon, 2012;Jenkins et al, 2007;Lawlor, 1982;Lomolino, 1984Lomolino, , 1985McDowall, Mitchell, & Brothers, 1994;Roff & Fairbairn, 2001). Several lines of evidence indicate that also vertebral number (henceforth VN) is associated with maneuverability and speed of locomotion (Arnold, 1988;Arnold & Bennett, 1988;Kelley, Arnold, & Glatstone, 1997;Long et al, 2011;McDowall, 2003;Swain, 1992a;Webb, 1975). For instance, VN influences body flexibility and the ability to curve the body (Ackerly & Ward, 2016;Brainerd & Patek, 1998).…”