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, 4 (5), e129

Molecular-level Variation Affects Population Growth in a Butterfly Metapopulation

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Molecular-level Variation Affects Population Growth in a Butterfly Metapopulation

Ilkka Hanski et al. PLoS Biol.

Abstract

The dynamics of natural populations are thought to be dominated by demographic and environmental processes with little influence of intraspecific genetic variation and natural selection, apart from inbreeding depression possibly reducing population growth in small populations. Here we analyse hundreds of well-characterised local populations in a large metapopulation of the Glanville fritillary butterfly (Melitaea cinxia), which persists in a balance between stochastic local extinctions and recolonisations in a network of 4,000 discrete habitat patches. We show that the allelic composition of the glycolytic enzyme phosphoglucose isomerase (Pgi) has a significant effect on the growth of local populations, consistent with previously reported effects of allelic variation on flight metabolic performance and fecundity in the Glanville fritillary and Colias butterflies. The strength and the sign of the molecular effect on population growth are sensitive to the ecological context (the area and spatial connectivity of the habitat patches), which affects genotype-specific gene flow and the influence of migration on the dynamics of local populations. The biological significance of the results for Pgi is underscored by lack of any association between population growth and allelic variation at six other loci typed in the same material. In demonstrating, to our knowledge for the first time, that molecular variation in a candidate gene affects population growth, this study challenges the perception that differential performance of individual genotypes, leading to differential fitness, is irrelevant to population dynamics. These results also demonstrate that the spatial configuration of habitat and spatial dynamics of populations contribute to maintenance of Pgi polymorphism in this species.

Figures

Figure 1
Figure 1. Population Growth Explained by Ecological Factors and Pgi Genotype
Population growth rate ( R) is plotted against the logarithm of population size ( N t; A), regional change in population sizes ( N trend; B), and Pgi genotype frequency F (C). In panel (C), populations in small ( A < 0.8 ha) and large habitat patches have been identified with closed (continuous line) and open symbols (broken line), respectively. For statistics, see Table 1.
Figure 2
Figure 2. Population Growth Explained by Habitat Patch Area and Pgi Genotypes in Isolated Habitat Patches, in which Population Dynamics Are Little Influenced by Immigration
The dependent variable in each panel is the residual growth rate ( R) from a regression of R against regional trend in population sizes ( N trend), which is explained by genotypic composition and habitat patch area in isolated patches ( S t < 15). (A and B) show R against the Pgi genotype frequencies F and D, respectively, in small ( A < 0.3 ha; closed symbols, continuous line) and large habitat patches (open symbols, broken line). (C) shows R against patch area in populations with F greater (closed symbols, continuous line) or smaller than 0.3 (open symbols, broken line), respectively, and (D) shows the same result for D. Statistics on F are given in Table 1. In (B and D), the interaction between D and ln A is significant ( p = 0.005; full model F 3,40 = 3.64, p < 0.02).
Figure 3
Figure 3. Cumulative Egg Production as a Measure of Reproductive Success of Females with and without the Pgi-f Allele
(A) Cumulative egg production of f (closed symbols) and non- f females (open symbols) in small (continuous lines) and large patches (broken lines) in the absence of migration, calculated with the assumptions explained in Materials and Methods. (B) Cumulative egg production of females from new (closed symbols) and old populations (open symbols) in the experiment of Hanski et al. [ 36]. (C) Same as (A) but with the effect of emigration included.
Figure 4
Figure 4. Pattern of Pgi Differentiation among Populations
The value of Pgi genotype frequency F in relation to landscape connectivity (A) and habitat patch area (B). Closed (continuous line) and open symbols (broken line) in (A) represent habitat patches smaller or greater than 0.3 ha and in (B) isolated ( S landscape < 3) and well-connected patches, respectively. A model with ln A, S landscape, and their interaction explains 14% of variation in F ( F = 5.00, p = 0.003, n = 73). The ln A * S landscape interaction ( t = 2.54, p = 0.01) and the main effects of ln A ( t = −2.95, p = 0.004) and S landscape ( t = −2.84, p = 0.006) are all significant. The effects of ln A, S landscape, and ln A * S landscape were also significant in a model including all populations regardless of their size but weighting the regression with the average population size for the years 1994–1996 ( F = 3.24, p = 0.02, n = 324; the p-values for the coefficients were 0.02, 0.01, and 0.03, respectively).

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