Inbreeding depression and differential maladaptation shape the fitness trajectory of two co-occurring Eucalyptus species

Abstract

& Key message The fitness trajectory of long-lived forest species with mixed mating systems is shaped by a dynamic interplay between endogenous (inbreeding depression) and exogenous (environmental maladaptation) factors. Using two eucalypt species, we show that the timing and translation of inbreeding depression from growth to survival through size-dependent mortality may vary between species and may intensify under climate stress. & Context Inbreeding is an important issue in evolutionary biology and breeding, as it can reduce genetic diversity and fitness and ultimately limit the adaptive response of populations to environmental stress. This is particularly relevant to forest tree species, such as eucalypts, which have a mixed mating system and long-generation intervals. & Aim Examine the role of inbreeding depression on the fitness trajectory of two eucalypt species, Eucalyptus globulus and E. ovata. & Methods Survival, growth, and reproduction of controlled-crossed self and outcross, as well as open-pollinated progeny of each species grown in a common garden field trial were assessed over a 28-year period and analysed using mixed effect models. & Results Inbreeding depression resulted in the purging of inbred progeny through size-dependent mortality with the most death of inbreds occurring between 4 and 13 years. After this period, differential maladaptation of the species was the dominant cause of mortality, associated with a period of drought and high temperatures, and it was evident first in the selfed populations. & Conclusion This study demonstrates the dynamic nature of the selective process in purging inbred progeny from a population, with inbreeding depression the dominant factor early in stand development, leading to older stands being dominated by outcrosses.

Conservation of old individual trees and small populations is integral to maintain species' genetic diversity of a historically fragmented woody perennial

“…Similarly, some populations of Eucalyptus globulus show high susceptibility to inbreeding depression, while purging of genetic load may reduce vulnerability to inbreeding depression in others including the relatively isolated King Island population of E. globulus that has low levels of heterozygosity (Costa e Silva et al, 2011;Steane et al, 2006). Thus, plant populations that vary in mating history may also display differences in the extent to which genetic variation impacts fitness (Keller & Waller, 2002;Nickolas, Harrison, Tilyard, Vaillancourt, & Potts, 2019).…”

Temperature and Rainfall Are Separate Agents of Selection Shaping Population Differentiation in a Forest Tree

“…The use of above-ground growth as a fitness surrogate has been suggested in long-lived species, such as forest trees, particularly at young stages when plants have not reached reproductive maturity [31,32]. Within eucalypt species, radial stem size (e.g., diameter or basal area) and tree height are usually highly positively correlated at the genetic and phenotypic levels [33] and for trees of the same cohort grown under competition, survival increases with radial stem size [34][35][36], consistent with size-dependent mortality [37]. Nevertheless, although HT growth 44 months after planting may be considered as a fitness surrogate in an early stage of a tree's life cycle, it will not necessarily represent a major component of lifetime fitness.…”

Divergent lineages in a semi‐arid mallee species, Eucalyptus behriana, correspond to a major geographic break in southeastern Australia

“…Similar patterns are seen in other widespread tree species with large population sizes across various regions of the world, including other Eucalyptus species (Bloomfield et al., 2011; Jones et al., 2013; Murray et al., 2019; Nevill, Bradbury, et al., 2014; Supple et al., 2018), Quercus (Ju et al., 2019), Populus (Keller et al., 2010), and Pinus (Potter et al., 2015), which show limited genetic structuring; with isolation by distance explaining much of the genetic divergence. In the case of eucalypts, it has been suggested that their high recombination rates (Gion et al., 2016), preferential outcrossing (Byrne, 2008; Horsley & Johnson, 2007), and substantial inbreeding depression in the case of selfing (Nickolas et al., 2019), all favor the retention of genetic diversity and a lack of geographical structuring despite lacking long distance dispersal capabilities (Booth, 2017).…”