Mycorrhizal divergence and selection against immigrant seeds in forest and dune populations of the partially mycoheterotrophicPyrola rotundifolia

Abstract

Plant populations occupying different habitats may diverge from each other over time and gradually accumulate genetic and morphological differences, ultimately resulting in ecotype or even species formation. In plant species that critically rely on mycorrhizal fungi, differences in mycorrhizal communities can contribute to ecological isolation by reducing or even inhibiting germination of immigrant seeds. In this study, we investigated whether the mycorrhizal communities available in the soil and associating with the roots of seedlings and adult plants of the partially mycoheterotrophic Pyrola rotundifolia differed between populations growing in sand dunes and forests. In addition, reciprocal germination experiments were performed to test whether native seeds showed higher germination than immigrant seeds. Our results showed that the mycorrhizal communities differed significantly between forest and dune populations, and that within populations seedlings and adults also associated with different mycorrhizal communities. In both forest and dune populations, mycorrhizal communities were dominated by members of the Thelephoraceae, but dune populations showed a higher incidence of members of the Inocybaceae, whereas forest populations showed a high abundance of members of the Russulaceae. Reciprocal germination experiments showed that native seeds showed a higher germination success than immigrant seeds and this effect was most pronounced in dune populations. Overall, these results demonstrate that plants of P. rotundifolia growing in dune and forest habitats associate with different mycorrhizal communities and that reduced germination of non‐native seeds may contribute to reproductive isolation. We conclude that selection against immigrants may constitute an important reproductive barrier at early stages of the speciation process.

Mycorrhizal symbioses and the evolution of trophic modes in plants

“…The few available studies have shown that, in some cases, mycorrhizal communities shift during ontogenetic development. For example, germinating seeds and the first underground stages of several Pyrola (Ericaceae) species have been shown to associate with multiple partners simultaneously, but the fungi that associated with seeds differed from those associating with adult plants (Hashimoto et al, ; Hynson, Weiss, Preiss, Gebauer, & Treseder, ; Jacquemyn, Waud, & Brys, ; Johansson, Bahram, Tedersoo, Kõljalg, & Eriksson, ), suggesting that plants may serially associate with different partners rather than specializing on a single ‘best’ partner. Similarly, the mycorrhizal communities associating with protocorms and adult plants of the orchid Liparis loeselii (Orchidaceae) were diverse and varied among life cycle stages (Waud, Brys, Landuyt, Lievens, & Jacquemyn, ).…”

‘Dust seeds’ with undifferentiated embryos and their germination in mycoheterotrophic Monotropoideae (Ericaceae)

“…Their idea was that the soil fungi differed between the two habitat types (populations), which they found it did, and that the fungi at one site would be more conducive to germination of its native seeds than to immigrant (nonnative) seeds from the other site. Overall, Jacquemyn et al (2018) found that natives germinated somewhat better than nonnatives. After 2 years of burial, there were, on average, more seedlings from native than from nonnative seeds in packets from five of the six subpopulations.…”

“…Jacquemyn et al (2018) compared the germination of seeds of P. rotundifolia during burial in a reciprocal seed transplant study between populations in an inland temperate deciduous forest and coastal sand dunes/dune slacks in Belgium. Native and nonnative seeds to the two populations were buried reciprocally for 2 years in three forest and three dune subpopulations (replicates).…”

“…Using data in Fig. 4 of Jacquemyn et al (2018), we calculated that 1344 seedlings germinated from the 42,000 seeds buried: (1344/42,000) × 100 = 3.2% germination. Considering that only 159 of 168 seed packets buried were retrieved increases germination a bit: 159 × 250 (seeds/packet) = 39,750 (seeds retrieved) and (1344/39,750) × 100 = 3.4% germination.…”

Chromosome-level genome assembly of the fully mycoheterotrophic orchid Gastrodia elata

“…Such mycorrhizal community changes during ontogenetic development have been shown in other species. For example, the fungi that associate with seeds of several Pyrola (Ericaceae family) species differ from those coupled with adult plants ( Hashimoto et al 2012 ; Hynson et al 2013 ; Johansson et al 2017 ; Jacquemyn et al 2018 ). This indicates that some plants may serially associate with different fungal partners rather than choosing a single best partner.…”