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Review
. 2019 Jan 23;123(2):337-345.
doi: 10.1093/aob/mcy144.

Does the evolution of self-fertilization rescue populations or increase the risk of extinction?

Affiliations
Review

Does the evolution of self-fertilization rescue populations or increase the risk of extinction?

P-O Cheptou. Ann Bot. .

Abstract

Background and aims: As a major evolutionary transition in seed plants, the evolution of plant mating systems has been much debated in evolutionary ecology. Over the last 10 years, well-established patterns of evolution have emerged. On the one hand, experimental studies have shown that self-fertilization is likely to evolve in a few generations (microevolution) as a response to rapid environmental change (e.g. pollinator decline), eventually rescuing a population. On the other, phylogenetic studies have demonstrated that repeated evolution towards self-fertilization (macroevolution) leads to a higher risk of lineage extinction and is thus likely to be disadvantageous in the long term.

Scope: In either case - the short-term or long-term evolution of self-fertilization (selfing) - these findings indicate that a mating system is not neutral with respect to population or lineage persistence. They also suggest that selfing can have contrasting effects depending on time scale. This raises the question of whether mating system evolution can rescue populations facing environmental change. In this review, empirical and theoretical evidence of the direct and indirect effects of mating systems on population demography and lineage persistence were analysed. A simple theoretical evolutionary rescue model was also developed to investigate the potential for evolutionary rescue through selfing.

Key findings: Demographic studies consistently show a short-term advantage of selfing provided by reproductive assurance, but a long-term disadvantage for selfing lineages, suggesting indirect genomic consequences of selfing (e.g. mutation load and lower adaptability). However, our theoretical evolutionary rescue model found that even in the short term, while mating system evolution can lead to evolutionary rescue, it can also lead to evolutionary suicide, due to the inherent frequency-dependent selection of mating system traits.

Conclusions: These findings point to the importance of analysing the demographic consequences of self-fertilization in order to predict the effect of selfing on population persistence as well as take into account the indirect genomic consequences of selfing. The pace at which processes such as inbreeding depression, purging, reproductive assurance and genomic rearrangements occur after the selfing transition is the key to clarifying whether or not selfing will result in evolutionary rescue.

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Figures

Fig. 1.
Fig. 1.
Shifts in anther–stigma distance in four experimental populations of Mimulus guttatus evolving with pollinators (white dots) or without pollinators (black dots) over five generations from initially equivalent populations (no dot). Reduced herkogamy is associated with the increase of selfed seed production. Error bars show standard errors (modified from Roels and Kelly, 2011, with permission).
Fig. 2.
Fig. 2.
Phylogenetic relationships in the Solanaceae species (356 species). Self-incompatibility (SI) and self-compatibility (SC) are depicted by purple and turquoise tips, respectively. Probability distribution of transitions (and 95 % credibility intervals) between characters. (A) Estimates of transition (q), extinction (μ) and speciation (λ) are given for SI species (I subscript) and SC species (C subscript). (B) The net diversification rate is the difference between speciation and extinction rates. (C) Summary of estimated parameters (taken from Goldberg et al., 2010, with permission).
Fig. 3.
Fig. 3.
Seed set and time to extinction in herkogamous and non-herkogamous plants of the species Gentianella campestris (from Lennartsson, 2002). The percentage of grassland in the landscape was 2–6 % for left panels and 12–15 % for right panels. Top: mean seed set (and standard deviation) in six populations along gradients of local fragmentation. Bottom: mean time to extinction for each local habitat fragment estimated from a stochastic matrix population model (see Lennartsson, 2002 for methodology, with permission).
Fig. 4.
Fig. 4.
Inbreeding depression estimates from the variation between self- fertilization in progeny (s =1− t) and the inbreeding coefficient (F) of adult R. ferrugineum individuals in 24 patches. The solid line indicates the relationship between s and F in patches at equilibrium in the absence of inbreeding depression. From the deviation of the curve, inbreeding depression expressed during the life cycle can be inferred, resulting in a mean (s.e.) life time estimate of ID in natura of 0.9±0.03 (see Delmas et al., 2014 for more details, with permission)
Fig. 5.
Fig. 5.
The evolution of self-fertilization towards a non-optimal population growth rate in a context of pollen limitation assuming that the evolution is driven by the Fisherian cost of outcrossing and inbreeding depression (δ) (without purging) and the pollination rate of outcrossed ovules (e). Complete self-fertilization evolves for the set of parameters below the solid line and complete outcrossing evolves for the set of parameters above the solid line. Increased growth by selfing occurs below the thin line, resulting in evolutionary rescue, and decreased growth by selfing occurs above the thin line, resulting in evolutionary suicide.

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