Contrasting Latitudinal Variations in Vertebral Number and Sex Determination in Pacific Versus Atlantic Silverside Fishes
Organisms that are distributed across spatial climate gradients often exhibit adaptive local variations in morphological and physiological traits, but to what extent such gradients shape evolutionary responses is still unclear. Given the strong natural contrast in latitudinal temperature gradients between the North-American Pacific and Atlantic coast, we asked how increases in vertebral number (VN, known as Jordan's Rule) with latitude would differ between Pacific (Atherinops affinis) and Atlantic Silversides (Menidia menidia), two ecologically equivalent and taxonomically similar fishes with similar latitudinal distributions. VN was determined from radiographs of wild-caught adults (genetic + environmental differences) and its genetic basis confirmed by rearing offspring in common garden experiments. Compared to published data on VN variation in M. menidia (a mean increase of 7.0 vertebrae from 32 to 46°N, VN slope = 0.42 lat−1), the latitudinal VN increase in Pacific Silversides was approximately half as strong (a mean increase of 3.3 vertebrae from 28 to 43°N, VN slope = 0.23 lat−1). This mimicked the strong Atlantic (1.11°C lat−1) versus weak Pacific latitudinal gradient (0.40°C lat−1) in median annual sea surface temperature (SST). Importantly, the relationship of VN to SST was not significantly different between the two species (average slope = −0.39 vertebrae °C−1), thus suggesting a common thermal dependency of VN in silverside fishes. Our findings provide novel support for the hypothesis that temperature gradients are the ultimate cause of Jordan's Rule, even though its exact adaptive significance remains speculative. A second investigated trait, the mode of sex determination in Atlantic versus Pacific Silversides, revealed patterns that were inconsistent with our expectation: M. menidia displays temperature-dependent sex determination (TSD) at low latitudes, where growing seasons are long or unconstrained, but also a gradual shift to genetic sex determination (GSD) with increasing latitude due to more and more curtailed growing seasons. Sex ratios in A. affinis, on the other hand, were independent of latitude and rearing temperature (indicating GSD), even though growing seasons are thermally unconstrained across most of the geographical distribution of A. affinis. This suggests that additional factors (e.g., longevity) play an important role in shaping the mode of sex determination in silverside fishes.
Long-term SST patterns along the North-American Atlantic and Pacific coasts derived from satellite and in situ measurements (1982–2008). Dots depict median SSTs, bars the range between minimum and maximum SSTs per year.
Atherinops affinis. Mean (± SD) vertebral number of field-collected mature adults from four populations along the North-American Pacific coast (P128°N–P443°N). Gray circles denote the data range, black circles and error bars are population means ± 1 SD. Dotted lines depict 10th and 90th percentiles. Sample sizes are given in parentheses next to each population, asterisks identify significant differences (P < 0.05) between adjacent populations (ns = non-significant).
Atherinops affinis. Latitudinal variation in vertebral number in offspring from four populations (P128°N–P443°N) reared at three temperatures in common garden experiments (A: 15°C, B: 21°C, C: 27°C). Black circles and error bars represent population means ± 1 SD. Dotted lines depict 10th and 90th percentiles. Sample sizes are given in parentheses, asterisks identify significant differences (P < 0.05) between adjacent populations (ns = non-significant).
Atherinops affinis. Mean (± SD) number of vertebrae for juveniles of four populations (P128°N–P443°N) reared at 15, 21, and 27°C. Asterisks denote significant differences (P < 0.05) between adjacent temperature treatments.
Latitudinal variation in vertebral number in field-caught Atlantic versus Pacific Silverside populations. (A) Population means ± 1 SD for Atherinops affinis (Aa, this study), Menidia menidia (Mm, compiled from Billerbeck et al., 1997 [white circles: material collected 1986, gray circles: material collected 1988/89]; Yamahira et al., 2006), and M. peninsulae (Mp, compiled from Yamahira et al., 2006). (B) Least squares regression lines and 95% confidence intervals for Aa (b95%Aa = 0.17–0.30), Mm (b95%Mm = 0.37–0.47), and Mp (b95%Mp = 0.14–1.18), based on the data shown in panel A.
Relationship between temperature and vertebral number (VN) for Atlantic (Menidia menidia, black circles) and Pacific Silverside fishes (Atherinops affinis, empty diamonds). Mean VNs of field caught, mature individuals were regressed against median annual SSTs at coastal latitudes corresponding to the origin of each population (extracted from a long-term data set of satellite and in situ observations, publicly available at http://dss.ucar.edu/datasets/ds277.0). Black dashed lines depict 95% confidence intervals. The slopes of the two relationships (M. menidia: VN = 46.1–0.30*SST, r2 = 0.91; A. affinis: VN = 54.0–0.48*SST, r2 = 0.91) were not significantly different (ANCOVA, P = 0.81, Table 2).
Atherinops affinis. Sex ratios of juveniles from four spatially distinct populations (P128°N–P443°N) reared from the egg stage at three temperatures in 2008 and 2009. Absolute numbers of males (black letters) and females (white letters) are given in each bar.
Contributor Notes
Associate Editor: T. Grande.