Life stage-specific inbreeding depression in long-lived Pinaceae species depends on population connectivity

Jon Ahlinder,M Rosario García-Gil,Barbara E Giles

doi:10.1038/s41598-021-88128-4

Jon Ahlinder, M Rosario García-Gil + Show 1 more

Open Access

https://doi.org/10.1038/s41598-021-88128-4

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Abstract

Inbreeding depression (ID) is a fundamental selective pressure that shapes mating systems and population genetic structures in plants. Although it has been shown that ID varies over the life stages of shorter-lived plants, less is known about how the fitness effects of inbreeding vary across life stages in long-lived species. We conducted a literature survey in the Pinaceae, a tree family known to harbour some of the highest mutational loads ever reported. Using a meta-regression model, we investigated distributions of inbreeding depression over life stages, adjusting for effects of inbreeding levels and the genetic differentiation of populations within species. The final dataset contained 147 estimates of ID across life stages from 41 studies. 44 Fst estimates were collected from 40 peer-reviewed studies for the 18 species to aid genetic differentiation modelling. Partitioning species into fragmented and well-connected groups using Fst resulted in the best way (i.e. trade-off between high goodness-of-fit of the model to the data and reduced model complexity) to incorporate genetic connectivity in the meta-regression analysis. Inclusion of a life stage term and its interaction with the inbreeding coefficient (F) dramatically increased model precision. We observed that the correlation between ID and F was significant at the earliest life stage. Although partitioning of species populations into fragmented and well-connected groups explained little of the between-study heterogeneity, the inclusion of an interaction between life stage and population differentiation revealed that populations with fragmented distributions suffered lower inbreeding depression at early embryonic stages than species with well-connected populations. There was no evidence for increased ID in late life stages in well-connected populations, although ID tended to increase across life stages in the fragmented group. These findings suggest that life stage data should be included in inbreeding depression studies and that inbreeding needs to be managed over life stages in commercial populations of long-lived plants.

Highlights

Inbreeding depression (ID) is a fundamental selective pressure that shapes mating systems and population genetic structures in plants
ID data for 18 species from five genera (Pinus, Abies, Picea, Pseudotsuga and Larix) in the Pinaceae were obtained from 41 studies (Figs. 1, 2, Fig. S1, Table S1), by using the Web of Science database as well as older reports held in plant breeding institutions
147 estimates of ID were included in the analysis, which makes this one of the more extensive compilations for long-lived perennial species reported in the literature

Summary

Introduction

Inbreeding depression (ID) is a fundamental selective pressure that shapes mating systems and population genetic structures in plants. Even fewer studies have addressed the question of how population size and genetic differentiation affect the strengths of ID across life stages of long-lived species This lack of knowledge is surprising given the long-standing recognition that tree species should be more favourable than short-lived species as models for studying the cumulative life stage effects of inbreeding on ID4,8. Should inbreeding continue in these small populations, selective elimination of the deleterious alleles (purging) is expected, leading to reduced levels of ID as observed in species with self-fertilising mating systems. In small populations affected by a longer histories of inbreeding, crossing experiments designed to measure ID in these populations may fail to detect further reductions in population fitness (ID baseline hypothesis)13 This could lead to the erroneous inference that the apparently low levels of ID were caused by purging (purging hypothesis). The major force counteracting a transmission advantage of selfing is lost and breeding systems will evolve to allow greater levels of inbreeding or selfing, which would not be the case under the ID baseline hypothesis

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