Life-history plasticity in female threespine stickleback

Abstract

The postglacial adaptive radiation of the threespine stickleback fish (Gasterosteus aculeatus) has been widely used to investigate the roles of both adaptive evolution and plasticity in behavioral and morphological divergence from the ancestral condition represented by present-day oceanic stickleback. These phenotypes tend to exhibit high levels of ecotypic differentiation. Population divergence in life history has also been well studied, but in contrast to behavior and morphology, the extent and importance of plasticity has been much less well studied. In this review, we summarize what is known about life-history plasticity in female threespine stickleback, considering four traits intimately associated with reproductive output: age/size at maturation, level of reproductive effort, egg size and clutch size. We envision life-history plasticity in an iterative, ontogenetic framework, in which females may express plasticity repeatedly across each of several time frames. We contrast the results of laboratory and field studies because, for most traits, these approaches give somewhat different answers. We provide ideas on what the cues might be for observed plasticity in each trait and, when possible, we inquire about the relative costs and benefits to expressed plasticity. We end with an example of how we think plasticity may play out in stickleback life history given what we know of plasticity in the ancestor.

Figure 1

Size frequency of age-1 female threespine stickleback in Cornelius Lake, Alaska. Solid bars indicate nonbreeding females, confirmed by dissection; hatched bars indicate females that were in the clutch-production cycle (Baker et al., 1998). Breeders are clearly primarily the larger fish, although size is not a perfect predictor, as some larger fish are not breeders. The main group of breeding females in this population are age-2 individuals.

Figure 2

Size frequency of anadromous threespine stickleback on the breeding ground in two Alaskan populations. (a–c) Anchor River population 1995–1997. (d) Mud Lake population (Karve et al., 2013). All fish are reproductive females captured on the breeding grounds. The clear size modes in Anchor River represent age-1 and age-2 breeders; only age-2 breeders make the extended migration up the Knik River system and tributaries to spawn in Mud Lake.

Figure 3

Comparison of compensatory responses in somatic mass and lipid content of threespine stickleback in experimental (DPR3) and control (CONT) fish that experienced a 50% reduction in ration in their fourth month of life (∼2 months before over-wintering). The left panels show values at the end of 1 month of reduced ration; the right panels show values after a return to full ration for 1 month. The magnitude of the differences between control and experimental fish for each panel is indicated by an effect size metric (Cohen's d).

Figure 4

The relationship between dry clutch mass (an indicator of reproductive effort) and female somatic mass in Big Beaver Lake, Alaska, 1997. Each symbol indicates an individual female. At the mean somatic mass of 0.90 g, female clutch mass can vary higher or lower by as much as one-third from the expected value along the regression line.

Figure 5

Relationships between clutch mass and body mass in female threespine stickleback from four populations studied in the wild (solid circles) and in the lab (open circles). (a) Lynne Lake, Alaska—limnetic body shape. (b) Cornelius Lake, Alaska—intermediate body shape. (c) Willow Lake, Alaska—benthic body shape. (d) Shown are clutch masses for stickleback from three distinct habitats within the Misty Lake ecosystem, British Columbia, adjusted to a common female mass of 2.45 g. In panels a–c, fish less than ~1 g are age 1 individuals.

Figure 6

(a) The distribution of population-level regression slopes (model II) for 65 Alaskan populations of threespine stickleback. A slope of >1 indicates that relative reproductive effort increases with size/age. (b) An example of a one population's relationship; each filled circle represents an individual female. A 99% bivariate probability ellipse is fitted to the data, with the model II regression trend indicated by a dashed line.

Figure 7

The relationship between egg size (mean dry mass) and female somatic mass (blotted, eviscerated) in four populations of Alaskan threespine stickleback. (a) Resurrection Bay marine; (b) Anchor River anadromous; (c) Daniels Lake fresh water; (d) Bear Paw Lake fresh water.

Figure 8

(a) The relationship between clutch size and female body size (3 years pooled) in the Solid Rock, Alaska, population. (b) The relationship between egg size and female body size in the same population for the same samples. Note that the oldest females (estimated to be age 4) produce appropriate clutches for their body size, but produce smaller eggs than expected.

Figure 9

Matrix plot showing the relationships between female life-history traits, body mass and somatic condition in Big Beaver Lake, Alaska. The 99% probability ellipses are plotted for each pairwise combination of traits. Correlations were based on log values for female somatic mass, clutch size, egg size and clutch mass. Condition was the residual from a regression of log somatic mass on log SL.