Genome‐wide genotyping estimates mating system parameters and paternity in the island species Tolpis succulenta

Abstract

Premise The mating system has profound consequences, not only for ecology and evolution, but also for the conservation of threatened or endangered species. Unfortunately, small populations are difficult to study owing to limits on sample size and genetic marker diversity. Here, we estimated mating system parameters in three small populations of an island plant using genomic genotyping. Although self‐incompatible (SI) species are known to often set some self‐seed, little is known about how “leaky SI” affects selfing rates in nature or the role that multiple paternity plays in small populations. Methods We generalized the BORICE mating system program to determine the siring pattern within maternal families. We applied this algorithm to maternal families from three populations of Tolpis succulenta from Madeira Island and genotyped the progeny using RADseq. We applied BORICE to estimate each individual offspring as outcrossed or selfed, the paternity of each outcrossed offspring, and the level of inbreeding of each maternal plant. Results Despite a functional self‐incompatibility system, these data establish T. succulenta as a pseudo‐self‐compatible (PSC) species. Two of 75 offspring were strongly indicated as products of self‐fertilization. Despite selfing, all adult maternal plants were fully outbred. There was high differentiation among and low variation within populations, consistent with a history of genetic isolation of these small populations. There were generally multiple sires per maternal family. Twenty‐two percent of sib contrasts (between outcrossed offspring within maternal families) shared the same sire. Conclusions Genome‐wide genotyping, combined with appropriate analytical methods, enables estimation of mating system and multiple paternity in small populations. These data address questions about the evolution of reproductive traits and the conservation of threatened populations.

How rapidly do self‐compatible populations evolve selfing? Mating system estimation within recently evolved self‐compatible populations of Azorean Tolpis succulenta (Asteraceae)

“…Recent mating system estimation using field collected progeny sets from two populations on Madeira confirm predominant outcrossing (Gibson et al, 2020). However, despite a functional SI system, two of the 75 offspring scored in that study were confirmed as products of self-fertilization (Gibson et al, 2020). Crawford et al (2019) recently documented a breeding system shift from SI to SC within T. succulenta from the Azorean island of Graciosa ( Figure 2).…”

“…Gibson et al. (2020) discuss the advantages of the methods employed herein for studying the small populations of rare island plants. A major advantage, with conservation implications, is that mating system can be inferred because individual progeny can be called as selfed or outcrossed with few maternal families and few progeny per family.…”

“…The BORICE program (Colicchio et al., 2020) uses MCMC (Metropolis et al., 1953) to (a) estimate population outcrossing rates, (b) estimate maternal plant inbreeding coefficients, (c) ascertain whether progeny are selfed or outcrossed, and (d) assess single or multiple paternity of offspring (Gibson et al., 2020). BORICE was run with burn‐in of 1,000 and chain length of 4,000 steps.…”

“…The breeding system of Azorean T. succulenta is considered largely SI or PSC based on lack of or very low self‐seed set from two populations on two islands in the Azores (Crawford et al., 2015). Recent mating system estimation using field collected progeny sets from two populations on Madeira confirm predominant outcrossing (Gibson et al., 2020). However, despite a functional SI system, two of the 75 offspring scored in that study were confirmed as products of self‐fertilization (Gibson et al., 2020).…”

“…Recent mating system estimation using field collected progeny sets from two populations on Madeira confirm predominant outcrossing (Gibson et al., 2020). However, despite a functional SI system, two of the 75 offspring scored in that study were confirmed as products of self‐fertilization (Gibson et al., 2020).…”