Evolutionary processes in an undescribed eucalypt: implications for the translocation of a critically endangered species

Abstract

Background and aims: Knowledge of the evolutionary processes responsible for the distribution of threatened and highly localized species is important for their conservation. Population genomics can provide insights into evolutionary processes to inform management practices, including the translocation of threatened plant species. In this study, we focus on a critically endangered eucalypt, Eucalyptus sp. Cattai, which is restricted to a 40-km2 area of Sydney, Australia, and is threatened by increased urbanization. Eucalyptus sp. Cattai has yet to be formally described in part due to its suspected hybrid origin. Here, we examined evolutionary processes and species boundaries in E. sp. Cattai to determine whether translocation was warranted.

Methods: We used genome-wide scans to investigate the evolutionary relationships of E. sp. Cattai with related species, and to assess levels of genetic health and admixture. Morphological trait and genomic data were obtained from seedlings of E. sp. Cattai propagated in a common garden to assess their genetic provenance and hybrid status.

Key results: All analyses revealed that E. sp. Cattai was strongly supported as a distinct species. Genetic diversity varied across populations, and clonality was unexpectedly high. Interspecific hybridization was detected, and was more prevalent in seedlings compared to in situ adult plants, indicating that post-zygotic barriers may restrict the establishment of hybrids.

Conclusions: Multiple evolutionary processes (e.g. hybridization and clonality) can operate within one rare and restricted species. Insights regarding evolutionary processes from our study were used to assist with the translocation of genetically 'pure' and healthy ex situ seedlings to nearby suitable habitat. Our findings demonstrate that it is vital to provide an understanding of evolutionary relationships and processes with an examination of population genomics in the design and implementation of an effective translocation strategy.

Keywords: Latoangulatae; Symphyomyrtus; Clonality; genome-wide analysis; hybridization; self-compatibility; species boundaries; threatened species.

Fig. 1.

Morphology and distribution of Eucalyptus sp. Cattai, showing: (A) habit, buds, flowers and fruits, (B) distribution of red mahoganies in Australasia (subgenus Symphyomyrtus section Latoangulatae series Annulares, sensuBrooker, 2000), and (C) distribution of E. sp. Cattai and red mahoganies in the Sydney region. Photography by T. C. Wilson and S. Rutherford. Maps were created using the R package ‘leaflet’ and distribution data were obtained from the Australasian Virtual Herbarium (2021).

Fig. 2.

Relationships among Eucalyptus sp. Cattai and other eucalypts derived from genome-wide scans in: (A) Splitstree and (B) SVDquartets phylogeny. The analysis in A is based on 13 054 SNPs and includes all samples (codes are given in Table 1). In A, ‘Putative hybrids A’ includes seedlings from the Logie–Robson Road intersection; while those labelled as ‘Putative hybrids B’ consist of E. notabilis × E. resinifera, seedlings and one adult from Clarke Way, and seedlings from Saltwater Circle and Shoplands Road. The phylogeny in B includes all species sampled, with E. piperita and E. sieberi (Eucalyptus subgenus Eucalyptus) used as outgroup species. Putative hybrids identified in A and all seedlings were excluded from the analysis in B. In B, taxonomic sections (sec.) and series (ser.) in subgenus Symphyomyrtus (sensuNicolle and Jones, 2018) are shown and numbers above the branches represent bootstrap values >50 %.

Fig. 3.

Principal component analysis (PCA) showing groupings of Eucalyptus sp. Cattai populations based on genome-wide scans (5080 SNPs). Seedling and adult samples are indicated. Codes are given in Table 1.

Fig. 4.

TreeMix analysis of Eucalyptus sp. Cattai and other eucalypt species based on genome-wide SNP data showing the maximum-likelihood (ML) tree inferred under two migration events. Gene flow is indicated by arrows coloured yellow to red according to their weight (0–50 %). The corresponding residual matrix is presented in Supplementary Data Fig. S4. Codes are given in Table 1.

Fig. 5.

Seedlings of Eucalyptus sp. Cattai showing: (A) a genetically ‘pure’ individual from Shoplands Road, (B) a hybrid from Saltwater Circle and (C) a hybrid from Shoplands Road; (D) principal component analysis (PCA) biplot based on 13 morphological traits (Fig. S6). The hybrid in B is morphologically similar to the genetically pure individual of E. sp. Cattai shown in A, while leaves of the hybrid in C are visibly larger than in the pure individual. Genet type and sample codes of each seedling in D are provided in Supplementary Data Table S7. Photography by T. C. Wilson.

Fig. 6.

Pairwise kinship analysis of Eucalyptus sp. Cattai showing samples from (A) the Logie–Robson Road intersection (Log), Georgia Terrace (Geo), Bannerman Road (Ba), Colbran Avenue (Col), Clarke Way (Cla), Woodlands Road (Woo) and Shoplands Road (Sho); and (B) Saltwater Circle (Sa) only. The heatmap displays kinship estimates for each pair of samples for each site, with red corresponding to the highest kinship (≥0.40 = clone), orange-yellow corresponding to medium pairwise kinship coefficients (>0.25 and <0.40 = sibling), and white corresponding to the lowest kinship (0). The descending red diagonal is the result of an individual matched with itself. Coloured boxes highlight samples that belong to genets of multiple ramets, and the labels adjacent to each box indicate genet type and name (given in Supplementary Data Table S7). In B individuals that belong to genets of multiple ramets (Sa1 to Sa8) are labelled in the kinship heatmap and the locations of the adults are indicated as triangles in the map. Genets made up of a single ramet are shown as white squares in the map.

Fig. 6.

Pairwise kinship analysis of Eucalyptus sp. Cattai showing samples from (A) the Logie–Robson Road intersection (Log), Georgia Terrace (Geo), Bannerman Road (Ba), Colbran Avenue (Col), Clarke Way (Cla), Woodlands Road (Woo) and Shoplands Road (Sho); and (B) Saltwater Circle (Sa) only. The heatmap displays kinship estimates for each pair of samples for each site, with red corresponding to the highest kinship (≥0.40 = clone), orange-yellow corresponding to medium pairwise kinship coefficients (>0.25 and <0.40 = sibling), and white corresponding to the lowest kinship (0). The descending red diagonal is the result of an individual matched with itself. Coloured boxes highlight samples that belong to genets of multiple ramets, and the labels adjacent to each box indicate genet type and name (given in Supplementary Data Table S7). In B individuals that belong to genets of multiple ramets (Sa1 to Sa8) are labelled in the kinship heatmap and the locations of the adults are indicated as triangles in the map. Genets made up of a single ramet are shown as white squares in the map.