Can functional genomic diversity provide novel insights into mechanisms of community assembly? A pilot study from an invaded alpine streambed

Abstract

An important focus of community ecology, including invasion biology, is to investigate functional trait diversity patterns to disentangle the effects of environmental and biotic interactions. However, a notable limitation is that studies usually rely on a small and easy-to-measure set of functional traits, which might not immediately reflect ongoing ecological responses to changing abiotic or biotic conditions, including those that occur at a molecular or physiological level. We explored the potential of using the diversity of expressed genes-functional genomic diversity (FGD)-to understand ecological dynamics of a recent and ongoing alpine invasion. We quantified FGD based on transcriptomic data measured for 26 plant species occurring along adjacent invaded and pristine streambeds. We used an RNA-seq approach to summarize the overall number of expressed transcripts and their annotations to functional categories, and contrasted this with functional trait diversity (FTD) measured from a suite of characters that have been traditionally considered in plant ecology. We found greater FGD and FTD in the invaded community, independent of differences in species richness. However, the magnitude of functional dispersion was greater from the perspective of FGD than from FTD. Comparing FGD between congeneric alien-native species pairs, we did not find many significant differences in the proportion of genes whose annotations matched functional categories. Still, native species with a greater relative abundance in the invaded community compared with the pristine tended to express a greater fraction of genes at significant levels in the invaded community, suggesting that changes in FGD may relate to shifts in community composition. Comparisons of diversity patterns from the community to the species level offer complementary insights into processes and mechanisms driving invasion dynamics. FGD has the potential to illuminate cryptic changes in ecological diversity, and we foresee promising avenues for future extensions across taxonomic levels and macro-ecosystems.

Keywords: RNA‐seq; alien; alpine; community genomics; functional trait; gene expression; invasive; transcriptome.

FIGURE 1

Photographs of the invaded and pristine communities sampled at the Jardin Alpin du Lautaret, France. (a) Venn diagram comparing the observed species richness between the invaded and pristine communities. (b) Venn diagram comparing the functional genomic diversity (FGD) measured by the total number of unigenes from all species sampled from the invaded (N = 20; 7 alien and 13 native) and the pristine community (N = 16; 10 shared with the invaded community). Species are separated by provenance in the invaded or pristine community to illustrate differences between aliens and natives. (c) The number of distinct unigenes (and gene models) matching each functional GO slim category within the biological process, cellular component, and molecular function aspects recovered from the invaded (pink) or blue (pristine) communities

FIGURE 2

Overall comparison of phenotypic functional trait and functional genomic trait differences for alien (pink) and native (blue) species. Principal component analysis (PCA) showing dispersion of (a) functional phenotypic traits (FTD), and (b) functional genomic traits (FGD), defined by the number of unigenes associated with each GO slim category

FIGURE 3

Patterns of functional dispersion (y‐axis; unitless) calculated according to Laliberté and Legendre (2010) within the invaded (pink) and pristine (blue) community from (a) the perspective of different types of functional data, transcribed genes (FGD), and phenotypic traits (FTD), and (b) of transcribed genes within each GO aspect

FIGURE 4

FGD profiles for alien–native congeneric species pairs showing the proportion of distinct unigenes identified within each GO slim category (a‐c): Alchemilla mollis (alien)–Alchemilla xanthochlora (native); Caltha fistulosa (alien)–Caltha palustris (native); Heracleum mantegazzianum (alien)–Heracleum sphondylium (native); Ranunculus caucasicus (alien)–Ranunculus aconitifolius (native); and Ranunculus caucasicus (alien)–Ranunculus acris (native). Results from Fisher's exact test for significant differences between the proportion of unigenes in native versus alien congeners are reported to the left of each panel (NS = not significant; *p‐value < .05)

FIGURE 5

Relationship between differential expression (DE) measured by (a) the absolute value of median log 2 fold change in unigene expression (y = −0.01062x − 0.02486, adj. R ² = −0.1125, p‐value = .7717) or (b) the fraction of significantly differentially expressed unigenes (y = 1.45037x − 0.08958, adj. R ² = 0.1152, p‐value = .1787), and the difference in relative abundance of each native species grown in the invaded versus pristine communities