Plant traits correlated with generation time directly affect inbreeding depression and mating system and indirectly genetic structure

Abstract

Background: Understanding the mechanisms that control species genetic structure has always been a major objective in evolutionary studies. The association between genetic structure and species attributes has received special attention. As species attributes are highly taxonomically constrained, phylogenetically controlled methods are necessary to infer causal relationships. In plants, a previous study controlling for phylogenetic signal has demonstrated that Wright's FST, a measure of genetic differentiation among populations, is best predicted by the mating system (outcrossing, mixed-mating or selfing) and that plant traits such as perenniality and growth form have only an indirect influence on FST via their association with the mating system. The objective of this study is to further outline the determinants of plant genetic structure by distinguishing the effects of mating system on gene flow and on genetic drift. The association of biparental inbreeding and inbreeding depression with population genetic structure, mating system and plant traits are also investigated.

Results: Based on data from 263 plant species for which estimates of FST, inbreeding (FIS) and outcrossing rate (tm) are available, we confirm that mating system is the main influencing factor of FST. Moreover, using an alternative measure of FST unaffected by the impact of inbreeding on effective population size, we show that the influence of tm on FST is due to its impact on gene flow (reduced pollen flow under selfing) and on genetic drift (higher drift under selfing due to inbreeding). Plant traits, in particular perenniality, influence FST mostly via their effect on the mating system but also via their association with the magnitude of selection against inbred individuals: the mean inbreeding depression increases from short-lived herbaceous to long-lived herbaceous and then to woody species. The influence of perenniality on mating system does not seem to be related to differences in stature, as proposed earlier, but rather to differences in generation time.

Conclusion: Plant traits correlated with generation time affect both inbreeding depression and mating system. These in turn modify genetic drift and gene flow and ultimately genetic structure.

Figure 1

Mean values of t_m, F_IS and F_ST as a function of growth form (H: herbaceous, W: woody), perenniality (SL: short-lived, LL: long-lived), the combination of growth form and perenniality (H/SL: herbaceous short-lived, H/LL: herbaceous long-lived, W/LL: woody long-lived), the mode of pollen dispersal (A: abiotic, B: biotic) and outcrossing rate (MS: mixed mating species, AS: allogamous species). For each category the P-value associated with the statistical test is indicated by *** P < 0.001, ** 0.001<P < 0.01, * 0.01<P < 0.05 and ^NS for P > 0.05. At the left part of the slash the P-value corresponds to the TIPs test and at the right to the PICs test. "--" indicates an absence of statistical test. Standard error values for each category is available in the additional file 3.

Figure 2

Distribution of t_m, F_IS and F_ST according to growth form, perenniality and pollination mode categories (percentile versus ranked t_m-estimate, F_IS-estimate and F_ST-estimate data).

Figure 3

Conventional regressions analyses (TIPs) on the left and phylogenetically-controlled regression analyses (PICs) on the right, among plant traits: growth form, perenniality, pollination mode and stature. *** P < 0.001, ** 0.001<P < 0.01, * 0.01<P < 0.05 and ^NS for P > 0.05.

Figure 4

Distribution of F_IS according to t_m. The open circles correspond to short-lived herbaceous species, the closed circles to long-lived herbaceous species and the crosses to woody species. The thick continuous line represents F_e, which is the expected F_IS based on the observed t_m, assuming a mixed-mating system at equilibrium without inbreeding depression. The other lines correspond to the best-fitting curves according to equation 1 after adjusting the level of inbreeding depression, δ, for short-lived herbaceous species (short-hatched line), perennial herbaceous species (long-hatched line) and woody species (continuous line).