Heterochronic shift in gene expression leads to ontogenetic morphological divergence between two closely related polyploid species

Abstract

Heterochrony-alteration to the rate or timing of development-is an important mechanism of trait differentiation associated with speciation. Heterochrony may explain the morphological divergence between two polyploid species, June sucker (Chasmistes liorus) and Utah sucker (Catostomus ardens). The larvae of both species have terminal mouths; however, as adults, June sucker and Utah sucker develop subterminal and ventral mouths, respectively. We document a difference in the timing of shape development and a corresponding change in the timing of gene expression, suggesting the distinctive mouth morphology in June suckers may result from paedomorphosis. Specifically, adult June suckers exhibit an intermediate mouth morphology between the larval (terminal) and ancestral (ventral) states. Endemic and sympatric Chasmistes/Catostomus pairs in two other lakes also are morphologically divergent, but genetically similar. These species pairs could have resulted from the differential expression of genes and corresponding divergence in trait development. Paedomorphosis may lead to adaptive diversification in Catostomids.

Keywords: Animal morphology; Evolutionary Developmental Biology; Transcriptomics.

Graphical abstract

Figure 1

Head shape undergoes a shorter developmental sequence in June sucker Results of geometric morphometric analysis of head shape. (A) Thin plate spline deformations from positive and negative extremes of relative warps 1 and 2. (B) Least squares means of head shape by week for June sucker, Utah Lake Utah sucker, and Strawberry Reservoir Utah sucker on relative warps 1 and 2. (C) Least squares means (error bars represent 95% confidence intervals of the mean) for each sucker lineage on the 9 relative warps from the multivariate linear mixed model of head shape variation at week 14. (D) Thin plate spline deformations of divergence in head shape between sucker lineages at week 14. UL = Utah Lake, SR = Strawberry Reservoir.

Figure 2

Premaxilla shape is different between lineages after 14 weeks of development Results of geometric morphometric analysis of premaxilla shape. (A) Thin plate splines deformations from positive and negative extremes of relative warps 1 and 2. (B) Least squares means of premaxilla shape by week for June sucker, Utah Lake Utah sucker and Strawberry Reservoir Utah sucker on relative warps 1 and 2. (C) Least squares means (error bars represent 95% confidence intervals of the mean) for each sucker lineage on the 6 relative warps from the multivariate linear mixed model of premaxilla shape variation at week 14. (D) Thin plate spline deformations of divergence in premaxilla shape between lineages at week 14. UL = Utah Lake, SR = Strawberry Reservoir.

Figure 3

Premaxilla size undergoes a shorter developmental sequence in June sucker Plot of mean total limb length of the premaxilla (error bars represent 95% confidence intervals of the mean).

Figure 4

General transcript expression patterns are consistent with shorter development in June sucker Venn diagrams of differentially expressed transcripts for all pairwise comparisons (9v12, 9v14, 12v14) for each lineage. Darker colors indicate a higher numbers of differentially expressed transcripts.

Figure 5

Mouth development genes are only differentially expressed in Utah sucker lineages Plots of the transcript-level expression of mmp2 (represented by two transcripts) and nipbla.