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

Abstract

In plants where seed dispersal is limited compared with pollen dispersal, hybridisation may enhance gene exchange and species dispersal. We provide genetic evidence of hybridisation contributing to the expansion of the rare Eucalyptus risdonii into the range of the widespread Eucalyptus amygdalina. These closely related tree species are morphologically distinct, and observations suggest that natural hybrids occur along their distribution boundaries and as isolated trees or in small patches within the range of E. amygdalina. Hybrid phenotypes occur outside the range of normal dispersal for E. risdonii seed, yet in some hybrid patches small individuals resembling E. risdonii occur and are hypothesised to be a result of backcrossing. Using 3362 genome‐wide SNPs assessed from 97 individuals of E. risdonii and E. amygdalina and 171 hybrid trees, we show that (i) isolated hybrids match the genotypes expected of F1/F2 hybrids, (ii) there is a continuum in the genetic composition among the isolated hybrid patches from patches dominated by F1/F2‐like genotypes to those dominated by E. risdonii‐backcross genotypes, and (iii) the E. risdonii‐like phenotypes in the isolated hybrid patches are most‐closely related to proximal larger hybrids. These results suggest that the E. risdonii phenotype has been resurrected in isolated hybrid patches established from pollen dispersal, providing the first steps in its invasion of suitable habitat by long‐distance pollen dispersal and complete introgressive displacement of E. amygdalina. Such expansion accords with the population demographics, common garden performance data, and climate modelling which favours E. risdonii and highlights a role of interspecific hybridisation in climate change adaptation and species expansion.

Evolutionary Processes Shaping Postglacial Gene Pools of High-Altitude Forests: Evidence from the Endemic Eucalypts of Tasmania

“…In many forest tree systems, the most effective adaptive gene flow will most likely be gene flow among locally adapted populations and entail long-distance dispersal, which is more a function of pollen than seed [4,112,113]. However, it may also be facilitated when pollen-mediated gene flow extends to networks of proximal hybridising species [15,150], as is likely in the present case. The present and other studies suggest that such historical interspecific gene flow has been an important part of the evolutionary response to climate change in many forest tree systems [15].…”

“…There is also extensive chloroplast sharing and more or less continuous variation in phenotype and global admixture levels at the individual and population level in the Central Highlands encompassing E. archeri and both subspecies of E. gunnii, superimposed on clear adaptative differences between extreme populations. Such complex patterns of variation within a more or less continuous distribution highlights the blurred lines between populations, subspecies, and species in forest tree genera and the challenges in defining uniform and pragmatic criteria to define conservation units which adequately capture the genetic diversity and evolutionary processes in many systems [150,158].…”

Multi-Response Phylogenetic Mixed Models: Concepts and Application

“…This method has the obvious drawback of ignoring phylogenetic structure close to the tips (e.g., sister species relationships), modelling only those effects owing to deeper splits within the tree. However, in cases such as the Eucalypts, where taxonomic series often represent freely hybridising species groups (Pfeilsticker et al, 2023;Larcombe et al, 2015), modelling phylogenetic effects above the species level may in fact be desirable, as it relaxes the assumption that recent divergences can be expressed in terms of a strictly bifurcating evolutionary process.…”

Plant genome evolution in the genusEucalyptusdriven by structural rearrangements that promote sequence divergence

“…The ideal study group would be naturally evolving, have low prezygotic reproductive barriers, highly specious, and exist over a wide and variable evolutionary range. Eucalyptus with over 800 wild and undomesticated species that exist across a wide geographic and environmental range (Potts and Wiltshire, 1997; Booth et al ., 2015; Supple et al ., 2018), retain a conserved karyotype (Grattapaglia et al ., 2015; Butler et al ., 2017), are pollinated by generalist pollinators (Pfeilsticker et al ., 2023), are capable of wide-ranging dispersal of genetic material (Bezemer et al ., 2016; Murray et al ., 2019), and span 50 million years of divergent evolution (Thornhill et al ., 2019) make an ideal genus to study plant genome evolution.…”