Adaptation in Unstable Environments and Global Gene Losses: Small but Stable Gene Networks by the May-Wigner Theory

Abstract

Although gene loss is common in evolution, it remains unclear whether it is an adaptive process. In a survey of seven major mangrove clades that are woody plants in the intertidal zones of daily environmental perturbations, we noticed that they generally evolved reduced gene numbers. We then focused on the largest clade of Rhizophoreae and observed the continual gene set reduction in each of the eight species. A great majority of gene losses are concentrated on environmental interaction processes, presumably to cope with the constant fluctuations in the tidal environments. Genes of the general processes for woody plants are largely retained. In particular, fewer gene losses are found in physiological traits such as viviparous seeds, high salinity, and high tannin content. Given the broad and continual genome reductions, we propose the May-Wigner theory (MWT) of system stability as a possible mechanism. In MWT, the most effective solution for buffering continual perturbations is to reduce the size of the system (or to weaken the total genic interactions). Mangroves are unique as immovable inhabitants of the compound environments in the land-sea interface, where environmental gradients (such as salinity) fluctuate constantly, often drastically. Extending MWT to gene regulatory network (GRN), computer simulations and transcriptome analyses support the stabilizing effects of smaller gene sets in mangroves vis-à-vis inland plants. In summary, we show the adaptive significance of gene losses in mangrove plants, including the specific role of promoting phenotype innovation and a general role in stabilizing GRN in unstable environments as predicted by MWT.

Keywords: adaptive evolution; gene loss; genome; mangrove; network stability; unstable environment.

Fig. 1.

Origination and gene family reduction of Rhizophoreae mangroves. The origination, among-genera divergence, and within-genus divergence of Rhizophoreae mangroves coincided with three climatic optimum events in the upper left panel. The estimated divergence times are displayed near the nodes, with bars representing 95% confidence intervals. The WGD event shared by Rhizophoreae is marked with a star. The gray dot represents the lower time boundary of the earliest fossil of the common ancestor of Rhizophoreae mangroves (47.8 Ma). Rhizophoreae mangroves are indicated with red font. De novo assembled genomes in this study are marked with asterisks. The upper left panel shows historical temperature changes over 65 Myr (modified from Zachos et al. 2008). Three climate warming events are highlighted. The right panel shows fewer duplicated genes in Rhizophoreae mangroves than in nonmangroves.

Fig. 2.

Extensive gene reduction in independent mangrove clades. The red circles on the phylogenetic tree represent independent origin events of seven mangrove clades, with mangrove plants marked in red. The right panel showed the total gene number of each species. The mangrove clade P. acidula experienced a recent species-specific WGD event and was marked in pink.

Fig. 3.

Gene loss and viviparous seed evolution of Rhizophoreae mangroves. a) Viviparous propagules of Rhizophoreae mangroves. From upper left to bottom right: B. gymnorhiza, Ceriops tagal, K. candel, and R. apiculata. The photo source is Mangrove iD e-book (Duke 2017). b) Loss of genes related to seed development in Rhizophoreae mangroves. Six genes that were lost in Rhizophoreae mangroves are shown. The right panel shows the gene copy number of LEA. c) Diagram showing the possible mechanisms of vivipary in Rhizophoreae mangroves. Expansion and contraction of genes involved in embryo development, seed maturation, and reserve accumulation. Genes circled by elliptical dotted lines have been lost in Rhizophoreae mangroves.

Fig. 4.

Molecular mechanisms of high tannin content in Rhizophoreae mangroves. a) Gene copy number evolution in the flavonoid biosynthesis pathway. The upper panel is a sketch map of the pathway. Genes that oxidize tannin or consume their precursors have fewer copies in Rhizophoreae mangroves and are highlighted in bold font. The bottom panel shows the copy number of LAC15, FNS II, and FLS genes in Rhizophoreae mangroves and nonmangroves. b) There is a higher tannin content in the stems and leaves of three Rhizophoreae mangroves than in C. pectinifolia. c) Expression of genes in the flavonoid biosynthesis pathway. The gene expression was first measured by TPM. TPM values of each species were then normalized to make a between-species comparison (Materials and Methods). Heatmap showing the normalized TPM values transformed into a Z-score. The gene grouping is consistent with the pathway in a).

Fig. 5.

Patterns of gene family reduction in Rhizophoreae mangroves. a) A decrease in gene numbers in Rhizophoreae mangroves positively correlates with gene number variability among inland plants. Copy number variability is measured using the CV (standard deviation/mean). b) GO term enrichments (in the Biological Process category) for gene families with fewer genes in Rhizophoreae mangroves. The GO terms with false discovery rates (FDRs) less than 0.05 are displayed. FDRs are calibrated using the Benjamini and Hochberg method. The Jaccard coefficient measures similarity between gene sets and is defined as the size of the intersection divided by the size of the union of gene sets. If the Jaccard similarity coefficient > 0.2 between two GO terms, an edge would be drawn to connect the GO terms. Thicker edges indicate stronger similarities. c) Comparison of gene loss between Rhizophoreae mangroves and C. pectinifolia. The numbers and colors of the branches represent the inferred loss rates per million years. The total number of gene loss events from the ancestor to present in a species is marked on the right side. The WGD events shared among Rhizophoreae are marked with stars on the branches. d) The Venn diagram represents the intersection of loss events for the four genera of Rhizophoreae mangroves. Colors from white to red indicate an increasing number of lost events.

Fig. 6.

The role of gene family reduction in increasing GRN stability. a) The GRN stability is affected by gene number and interaction strength. The probability of GRN stability was calculated in 1,000 simulations. The lines represent GRN with different standard deviations of A_ij, the off-diagonal element of the matrix. b to d) Gene and TE loss and GRN stability across saline environments. Expression of both TEs and genes is more stable in R. apiculata than in C. pectinifolia across salinity levels. The subset of genes in C. pectinifolia in d) represents the gene families with fewer members in Rhizophoreae mangroves, and salinity levels influence them more. The significance level of the differences in expression fold changes between mangrove and nonmangrove was tested using the Kolmogorov–Smirnov test (P < 10⁻¹⁵).