Ecological constraint, rather than opportunity, promotes adaptive radiation in three-spined stickleback (Gasterosteus aculeatus) on North Uist

Abstract

The context and cause of adaptive radiations have been widely described and explored but why rapid evolutionary diversification does not occur in related evolutionary lineages has yet to be understood. The standard answer is that evolutionary diversification is provoked by ecological opportunity and that some lineages do not encounter the opportunity. Three-spined sticklebacks on the Scottish island of North Uist show enormous diversification, which seems to be associated with the diversity of aquatic habitats. Sticklebacks on the neighboring island of South Uist have not been reported to show the same level of evolutionary diversity, despite levels of environmental variation that we might expect to be similar to North Uist. In this study, we compared patterns of morphological and environmental diversity on North and South Uist. Ancestral anadromous sticklebacks from both islands exhibited similar morphology including size and bony "armor." Resident sticklebacks showed significant variation in armor traits in relation to pH of water. However, North Uist sticklebacks exhibited greater diversity of morphological traits than South Uist and this was associated with greater diversity in pH of the waters of lochs on North Uist. Highly acidic and highly alkaline freshwater habitats are missing, or uncommon, on South Uist. Thus, pH appears to act as a causal factor driving the evolutionary diversification of stickleback in local adaptation in North and South Uist. This is consistent with diversification being more associated with ecological constraint than ecological opportunity.

Keywords: North Uist; South Uist; morphometric study; stickleback.

FIGURE 1

Sites for the collection of samples from 10 lochs in North Uist and 8 lochs in South Uist, Scotland [(a) Map of United Kingdom (b) Loch position in North Uist (c) Loch position in South Uist with road map (yellow), agricultural land (white), and moorland (green)]

FIGURE 2

The first two PCs of body armor traits for anadromous sticklebacks collected from North (ash, circle) and South (orange, triangle) Uist. Traits were plate count and residual values (from body length) of first dorsal spine length (X1st.DSL), second dorsal spine length (X2nd.DSL), pelvic spine length (PSL), length of pelvis (LPS), and height of pelvis (HPS). PC1 (35.2%) describes overall variation in armor, with positive loadings of all variables. PC2 (22.75%) mainly not only describes variation in plate count (positive loading) but also reflects negative loadings for LPS and PSL. Ellipses represent 95% confidence levels within each dataset

FIGURE 3

Mean standard length (±SE) of anadromous and resident fish shows little overall variation in size between North (ash, circle) and South Uist (orange, triangle) sticklebacks. Resident sticklebacks of North and South Uist were significantly smaller than the anadromous fish

FIGURE 4

(a) The first two principal components (PCs) of six body armor traits and standard length for resident sticklebacks of North Uist (circle) and South Uist (triangle). PC1 (71.3%) describes overall variation in spine length and pelvic size, while PC2 (13.8%) describes variation in plate number. Each dot represents a single fish in one of four pH groups: Freshwater high pH (red), freshwater low pH (green), neutral pH (turquoise), and saltwater high pH (purple). Ellipses describe 95% confidence intervals for each pH group. (b) Correlogram showing correlations between all measured armor traits including plate count, PC1, PC2, and standard length of North and South Uist resident fish. Blue color denotes positive correlations where shade of the square box indicates the strength of the correlation. Measured traits were as follows: first dorsal spine length (X1st.DSL), second dorsal spine length (X2nd.DSL), pelvic spine length (PSL), length of pelvis (LPS), and height of pelvis (HPS)

FIGURE 5

(a–f) mean (±SE) plate count (a) and standard length (b) and mean residual size (c–f) of five armor traits in 18 freshwater stickleback populations on North (circle) and South Uist (triangle)