Rapid wing size evolution in African fig flies (Zaprionus indianus) following temperate colonization

Abstract

Invasive species often encounter novel selective pressures in their invaded range, and understanding their potential for rapid evolution is critical for developing effective management strategies. Zaprionus indianus is an invasive drosophilid native to Africa that reached Florida in 2005 and likely re-establishes temperate North American populations each year. We addressed two evolutionary questions in this system: first, do populations evolve phenotypic changes in the generations immediately following colonization of temperate environments? Second, does Z. indianus evolve directional phenotypic changes along a latitudinal cline? We established isofemale lines from wild collections across space and time and measured twelve ecologically relevant phenotypes, using a reference population as a control. Z. indianus evolved smaller wings following colonization, suggesting early colonizers have larger wings, but smaller wings are favorable after colonization. No other phenotypes changed significantly following colonization or across latitudes, but we did see significant post-colonization changes in principal components of all phenotypes. We documented substantial laboratory evolution and effects of the laboratory environment across multiple phenotypes, emphasizing the importance of controlling for both possibilities when conducting common garden studies. Our results demonstrate the potential for rapid adaptation in Z. indianus, which could contribute to its success and expansion throughout invaded ecosystems.

Keywords: Invasive species; Zaprionus indianus; cline; local adaptation; phenotypic evolution.

Figure 1:. Overview of experimental design and timeline.

The diagram indicates the relative timing of fly capture and experimental assays for the post-colonization (orange), latitude (gray), and lab evolution (green) experiments. The post-colonization evolution experiment compares the phenotypes of isofemale lines captured early and late in the season. The lab evolution experiment compares phenotypes of lines captured early in the season after 3-4 generations of lab rearing and 7-8 generations of lab rearing. The latitude experiment compares lines collected from locations spanning 15° latitude in North America. The inbred control line (purple) serves as a reference to test for lab environment or assay variation between experiments conducted at different times.

Figure 2:. Z. indianus wing size evolves rapidly in the wild and in the lab.

Wing size is the geometric mean of the major and minor radii of an ellipse fitted to the wing. Early and late describe when the flies were assayed; for the lab evolution experiment, the same lines were assayed at two different generations. Points illustrate all individuals measured (n = 1079 total); boxplots show median and quantiles. Asterisks indicate Bonferroni-corrected P < 0.05 in a mixed effects linear model (see Table S1 for full model results).

Figure 3:. Post-colonization evolution, lab evolution, and lab environment effects for 12 phenotypes in Z. indianus.

The endpoint of each line shows the least-squared model-fitted mean for each timepoint and error bars show model standard errors. Wild-derived lines (orange) were collected in August (early season) and November (late season) and measured for each phenotype after 3-4 generations of laboratory culture. Lab evolution lines (green) were collected and measured in the early season and remeasured alongside the late season flies after several additional generations in the lab. Inbred controls (purple) are a single inbred line that was assayed alongside all experimental flies. Bold lines indicate significant differences between early and late season phenotypes in mixed-effects linear models after Bonferroni correction (see Table 2; Table S1).

Figure 4:. Limited latitudinal phenotypic variation in Z. indianus.

Points represent the mean of all individuals from each population for a given phenotype, and error bars represent standard error of the mean. No phenotypes showed significant changes with latitude in the final models after Bonferroni correction.

Figure 5:. Principal component analysis of phenotypes.

A) Principal components analysis for wild-derived flies caught early in the season, late in the season, and from four different latitudes (combined here for visual clarity). Each point represents one isofemale line. Triangles represent the inbred control line phenotyped alongside each group. Data ellipses were drawn using a multivariate t-distribution. B) PCA of the four latitudinal populations. C) Ordination plot for the 12 phenotypes used for the PCA; PCs were calculated using normalized line means for each phenotype from the combined seasonal and latitudinal experiments.