Rapid local adaptation linked with phenotypic plasticity

Abstract

Models of "plasticity-first" evolution are attractive because they explain the rapid evolution of new complex adaptations. Nevertheless, it is unclear whether plasticity can facilitate rapid microevolutionary change between diverging populations. Here, we show how plasticity may have generated adaptive differences in fecundity between neighboring wild populations of burying beetles Nicrophorus vespilloides. These populations occupy distinct Cambridgeshire woodlands that are just 2.5 km apart and that probably originated from a common ancestral population about 1000-4000 years ago. We find that populations are divergently adapted to breed on differently sized carrion. Adaptive differences in clutch size and egg size are associated with divergence at loci connected with oogenesis. The populations differ specifically in the elevation of the reaction norm linking clutch size to carrion size (i.e., genetic accommodation), and in the likelihood that surplus offspring will be lost after hatching. We suggest that these two processes may have facilitated rapid local adaptation on a fine-grained spatial scale.

Keywords: Burying beetles; Nicrophorus vespilloides; interspecific competition; local adaptation; niche expansion; phenotypic plasticity; plasticity‐led evolution.

Figure 1

(A) Body size and frequency distribution of field‐caught Nicrophorus spp., illustrated with box‐and‐whisker plots (left) and kernel density estimation (right). Points indicate outliers. (B and C) Temporal variation in abundance of N. vespilloides (left y‐axis) and the other Nicrophorus spp. (right y‐axis) per trap in (B) Gamlingay and (C) Waresley Woods. The values represent the mean ± SEM of data collected per trap at the same time each year. (D and E) Averaged relative abundance of Nicrophorus spp. per trap throughout the field seasons in (D) Gamlingay and (E) Waresley Woods.

Figure 2

Efficiency (%) of carcass use (total brood mass divided by carcass mass) of N. interruptus, N. investigator, and N. vespilloides from Gamlingay Wood and N. vespilloides from Waresley Wood. Values represent the mean ± SEM.

Figure 3

The effect of carcass size on (A and B) clutch size and (C and D) average egg volume produced by N. vespilloides. n = 27 Gamlingay N. vespilloides per carcass size treatment, and n = 37 Waresley N. vespilloides per carcass size treatment. (A) and (C) show reaction norms derived when siblings are exposed to Small and Large carcasses, with each line connecting siblings from the same brood; values in (B) and (D) represent the mean ± SEM of these reaction norms, so that population differences can more easily be seen.

Figure 4

Differentiation at putative oogenesis genes. (A) Scatterplot of PBS values for Waresley and Gamlingay in 2‐kb windows genome‐wide. Loci in the lower right hand of the figure show high differentiation in Waresley but not in Gamlingay. Loci with PBS scores greater than 0.05 are highlighted—Waresley = blue, Gamlingay = red, and Both = purple. Notable genes are annotated. (B) Sliding window analysis (window = 500 bp; slide = 100 bp) of PBS values at the 5HT receptor 2a‐like receptor. The peak PBS in Waresley (blue) falls in the last intron of the gene.

Figure 5

The effect of carcass size on the brood size produced by N. vespilloides (n = 46 Gamlingay N. vespilloides per carcass size treatment, and n = 62 Waresley N. vespilloides per carcass size treatment). (A) Reaction norms derived when siblings are exposed to Small and Large carcasses, with each line connecting siblings from the same brood; (B) Mean ± SEM of the values shown in (A), so that population differences can more easily be seen.