Cogradient Variation Research Articles

The Covariance between Genetic and Environmental Influences across Ecological Gradients

Patterns of phenotypic change across environmental gradients (e.g., latitude, altitude) have long captivated the interest of evolutionary ecologists. The pattern and magnitude of phenotypic change is determined by the covariance between genetic and environmental influences across a gradient. Cogradient variation (CoGV) occurs when covariance is positive: that is, genetic and environmental influences on phenotypic expression are aligned and their joint influence accentuates the change in mean trait value across the gradient. Conversely, countergradient variation (CnGV) occurs when covariance is negative: that is, genetic and environmental influences on phenotypes oppose one another, thereby diminishing the change in mean trait expression across the gradient. CnGV has so far been found in at least 60 species, with most examples coming from fishes, amphibians, and insects across latitudinal or altitudinal gradients. Traits that display CnGV most often involve metabolic compensation, that is, the elevation of various physiological rates processes (development, growth, feeding, metabolism, activity) to counteract the dampening effect of reduced temperature, growing season length, or food supply. Far fewer examples of CoGV have been identified (11 species), and these most often involve morphological characters. Increased knowledge of spatial covariance patterns has furthered our understanding of Bergmann size clines, phenotypic plasticity, species range limits, tradeoffs in juvenile growth rate, and the design of conservation strategies for wild species. Moreover, temporal CnGV explains some cases of an apparent lack of phenotypic response to directional selection and provides a framework for predicting evolutionary responses to climate change.

EXPERIMENTAL STUDIES OF ADAPTATION IN CLARKIA XANTIANA. I. SOURCES OF TRAIT VARIATION ACROSS A SUBSPECIES BORDER

Both genetic differentiation and phenotypic plasticity might be expected to affect the location of geographic range limits. Co-gradient variation (CoGV), plasticity that is congruent with genetic differentiation, may enhance performance at range margins, whereas its opposite, counter-gradient variation (CnGV) may hinder performance. Here we report findings of reciprocal transplant experiments intended to tease apart the roles of differentiation and plasticity in producing phenotypic variation across a geographic border between two plant subspecies. Clarkia xantiana ssp. xantiana and C. xantiana ssp. parviflora are California-endemic annuals that replace each other along a west–east gradient of declining precipitation. We analyzed variation in floral traits, phenological traits, and vegetative morphological and developmental traits by sowing seeds of 18 populations (six of ssp. xantiana and 12 of ssp. parviflora) at three sites (one in each subspecies' exclusive range and one in the subspecies' contact zone), in two growing seasons (an exceptionally wet El Niño winter and a much drier La Niña winter). Significant genetic differences between subspecies appeared in 11 of 12 traits, and differences were of the same sign as in nature. These findings are consistent with the hypothesis that selection is responsible for subspecies differences. Geographic variation within subspecies over part of the spatial gradient mirrored between-subspecies differences present at a larger scale. All traits showed significant plasticity in response to spatial and temporal environmental variation. Plasticity patterns ranged from spatial and temporal CoGV (e.g., in node of first flower), to spatial CnGV (e.g., in flowering time), to patterns that were neither CoGV nor CnGV (the majority of traits). Instances of CoGV may reflect adaptive plasticity and may serve to increase performance under year-to-year environmental variation and at sites near the subspecies border. However, the presence of spatial CnGV in some critical traits suggests that subspecies ranges may also be constrained by patterns of plasticity.

Phenotypic clines, plasticity, and morphological trade-offs in an intertidal snail.

Understanding the genetic and environmental bases of phenotypic variation and how they covary on local and broad geographic scales is an important goal of evolutionary ecology. Such information can shed light on how organisms adapt to different and changing environments and how life-history trade-offs arise. Surveys of phenotypic variation in 25 Littorina obtusata populations across an approximately 400-km latitudinal gradient in the Gulf of Maine revealed pronounced clines. The shells of snails from northern habitats weighed less and were thinner and weaker in compression than those of conspecifics from southern habitats. In contrast, body size (as measured by soft tissue mass) followed an opposite pattern; northern snails weighed more than southern snails. A reciprocal transplant between a northern and southern habitat revealed substantial plasticity in shell form and body mass and their respective measures of growth. Southern snails transplanted to the northern habitat produced lighter, thinner shells and more body mass than controls raised in their native habitat. In contrast, northern snails transplanted to the southern site produced heavier, thicker shells and less body mass than controls raised in their native habitat. Patterns of final phenotypic variation for all traits were consistent with cogradient variation (i.e., a positive covariance between genetic and environmental influences). However, growth in shell traits followed a countergradient pattern (i.e., a negative covariance between genetic and environmental influences). Interestingly, body growth followed a cogradient pattern, which may reflect constraints imposed by cogradient variation in final shell size and thickness. This result suggests the existence of potential life-history trade-offs associated with increased shell production. Differences in L. obtusata shell form, body mass, and their respective measures of growth are likely induced by geographic differences in both water temperature and the abundance of an invading crab predator (Carcinus maenas). Water temperatures averaged 6.8 degrees C warmer during the transplant experiment and C. maenas abundance is greater in the southern Gulf of Maine. Because both increased water temperature and crab effluent affect shell form in the same way, future experiments are needed to determine the relative importance of each. Nevertheless, it is clear that phenotypic plasticity has an important role in producing geographic variation in L. obtusata shell form. Moreover, the evolution of phenotypic plasticity in L. obtusata and other marine gastropods may be driven by architectural constraints imposed by shell form on body mass and growth.

CONTRASTING PATTERNS OF HERITABLE GEOGRAPHIC VARIATION IN SHELL MORPHOLOGY AND GROWTH POTENTIAL IN THE MARINE GASTROPOD BEMBICIUM VITTATUM: EVIDENCE FROM FIELD EXPERIMENTS.

Similar phenotypes do not always imply similar genotypes. In species distributed over a broad latitudinal range, geographical variation in morphological and life-history traits may reflect very different relations between genotypic and environmental effects on these traits. Patterns of selection among latitudinally separated sites may minimize phenotypic differences in life-history traits but promote phenotypic differences in form. Thus, for example, latitudinal variation in temperature often leads to genetically based metabolic differences that minimize differences in growth rate among populations at different latitudes (countergradient variation). However, variation in habitat experienced by the same populations may promote genetically based differences in shell form (cogradient variation). Few attempts have been made to assess simultaneously such mosaic effects of natural selection on the genetic basis of variation in both morphological and life-history traits among geographically separated populations. I quantified the extent to which widely separated populations of the rocky shore marine gastropod Bembicium vittatum exhibited genetic differences in shell shape, shell pattern, and growth rate. Bembicium vittatum occurs naturally at only three widely separated locations on the Western Australian coast. Individuals were transplanted from all three locations to a latitudinally intermediate site, where they were released in different pairwise combinations and allowed to reproduce. F1 offspring from crosses between same- or different-source parents were identified using allozyme markers. When grown in a common environment, offspring from same-source parents exhibited similar differences in shell shape and pattern, but dramatic differences in growth rates, compared to native populations. Genetic variation therefore exists for all three traits. Growth rates in the common environment were positively correlated with latitude of the source population, confirming the existence of countergradient variation for growth associated with metabolic compensation. In addition, for both shell shape and growth rate, hybrids exhibited phenotypes roughly midway between the same-source parents, suggesting that genetic differences have a large additive component. In contrast, when one parent had pigmented spots, the offspring also had spots, suggesting a strong dominance component to the genetic basis of shell pattern. Genetic differences therefore yield different morphological phenotypes but similar life-history phenotypes, among latitudinally distant populations, and confirm a pattern of mosaic evolution in B. vittatum.