Expansion of the rareEucalyptus risdoniiunder climate change through hybridization with a closely related species despite hybrid inferiority

Abstract

Background and aims Hybridisation is increasingly recognised as an integral part of the dynamics of species range expansion and contraction. Thus, it is important to understand the reproductive barriers between co-occurring species. Extending previous studies that argued that the rare Eucalyptus risdonii was expanding into the range of the surrounding E. amygdalina by both seed and pollen dispersal, we here investigate the long-term fitness of both species and their hybrids and whether expansion is continuing. Methods We assessed the survival of phenotypes representing a continuum between the two pure species in a natural hybrid swarm after 29 years, along with seedling recruitment. The performance of pure species as well as artificial and natural hybrids was also assessed over 28 years in a common garden trial. Key results In the hybrid zone, E. amygdalina adults showed greater mortality than E. risdonii and the current seedling cohort is still dominated by E. risdonii phenotypes. Morphologically intermediate individuals appeared to be the least fit. Similar results were observed after growing artificial first generation and natural hybrids alongside pure species families in a common garden trial. Here, the survival, reproduction, health and growth of the intermediate hybrids were significantly less than either pure species, consistent with hybrid inferiority, although this did not manifest until later reproductive ages. Among the variable progeny of natural intermediate hybrids, the most E. risdonii-like phenotypes were the most fit. Conclusions This study contributes to the increasing number of reports of hybrid inferiority in Eucalyptus, suggesting postzygotic barriers contribute to the maintenance of species integrity even between closely related species. However, with fitness rapidly recovered following backcrossing it is argued that hybridisation can still be an important evolutionary process, in the present case appearing to contribute to the range expansion of the rare E. risdonii in response to climate change.

Molecular insights into the dynamics of species invasion by hybridisation in Tasmanian eucalypts

“…The viability of the species resurrection process is also dependent on the fitness of the F 1 and backcross hybrids. While there is evidence of F 1 hybrid inferiority in the present case, the F 1 hybrids are reproductive, and fitness appears to be recovered rapidly in E. risdonii backcross phenotypes both ex situ (Pfeilsticker et al, 2022) and in the wild (Potts, 1986). Better performance or fitness of first‐generation backcross hybrids compared to F 1 and F 2 hybrids has similarly been reported in other species (Zhang et al, 2016), including Eucalyptus species (Costa e Silva et al, 2012).…”

“…Selection in favour of the pollen parent species is a key component of the mechanism of species expansion by long‐distance hybridisation (Figure 2d). There is evidence that the selective regime has been favouring E. risdonii over E. amygdalina for over half a century at Government Hills, and it is expanding its range (Pfeilsticker et al, 2022). The species is dominant on hot, drought‐prone north‐west facing slopes in south‐eastern Tasmania and the predictions of increase in temperature and aridity due to climate change (Feng & Fu, 2013; Sherwood & Fu, 2014) predict selection in favour of E. risdonii in the future.…”

“…After the pollen has reached distant E. amygdalina trees, the next critical step is the production of F 1 hybrids that can establish and reach maturity (Figure 2c). Artificial crosses between E. amygdalina and E. risdonii planted in a common garden has demonstrated the viability of F 1 hybrids and the potential of these to survive (e.g., for over 28 years) and become reproductive (Pfeilsticker et al, 2022). This is further evidenced by isolated intermediate genotypes sampled being reproductive in the wild (results not shown).…”

“…We showed clearly that the two isolated E. risdonii backcross (RH) phenotypes scattered in the E. amygdalina forest were E. risdonii backcross genotypes (i.e., result of intermediate tree backcrossed to E. risdonii ) rather than F 2 hybrids; similarly, in one of the isolated patches, the E. risdonii backcross phenotypes were all closely related to putative mothers with intermediate phenotypes/genotypes. Further, while closer to a source of E. risdonii pollen, sampling of open‐pollinated seed collected from intermediate phenotypes in the hybrid zone resulted in many E. risdonii backcross (58%) and E. risdonii phenotype seedlings (5%) (Pfeilsticker et al, 2022). Importantly, in terms of the resurrection hypothesis, we found several cases where plants in isolated hybrid patches which resembled E. risdonii in morphology (i.e., R phenotypes) were actually E. risdonii backcross genotypes and most closely related to larger intermediate or E. risdonii backcross putative mothers.…”

“…This species is endemic to the island of Tasmania, Australia, and morphology‐based studies showed that it is actively hybridising with the co‐occurring, widespread, and also endemic Eucalyptus amygdalina (Potts & Reid, 1988, 1990). While not sister taxa, the two species are phylogenetically closely related (Ladiges et al, 1983; Senior et al, 2016; Thornhill et al, 2019) belonging to the same taxonomic series (subgenus Eucalyptus series Radiatae ; Nicolle, 2021), but markedly different in their morphologies (Figure 1; Pfeilsticker et al, 2022; Potts & Reid, 1985). They co‐occur in rugged topography where E. risdonii replaces E. amygdalina on hot, dry north‐ to west‐ facing slopes (Potts & Reid, 1985).…”