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Genetic diversity and structure of the critically endangered Artocarpus annulatus, a crop wild relative of jackfruit (A. heterophyllus)

Dickinson L, Noble H, Gardner E, Puad ASA, Zakaria WNFW, Zerega NJC

PeerJ, 2020;8:e9897.
PMID: 33005490 DOI: 10.7717/peerj.9897

Limestone karsts of Southeast Asia can harbor high levels of endemism, but are highly fragmented, increasingly threatened, and their biodiversity is often poorly studied. This is true of the Padawan Limestone Area of Sarawak, Malaysia, home to the endemic Artocarpus annulatus, the closest known wild relative of two important and underutilized fruit tree crops, jackfruit (A. heterophyllus) and cempedak (A. integer). Identifying and conserving crop wild relatives is critical for the conservation of crop genetic diversity and breeding. In 2016 and 2017, five A. annulatus populations were located, and leaf material, locality information, and demographic data were collected. Microsatellite markers were used to assess genetic diversity and structure among populations, and to compare levels of genetic diversity to closely related congeneric species. Results indicate no evidence of inbreeding in A. annulatus, and there is no genetic structure among the five populations. However, diversity measures trended lower in seedlings compared to mature trees, suggesting allelic diversity may be under threat in the youngest generation of plants. Also, genetic diversity is lower in A. annulatus compared to closely related congeners. The present study provides a baseline estimate of A. annulatus genetic diversity that can be used for comparison in future studies and to other species in the unique limestone karst ecosystems. Considerations for in situ and ex situ conservation approaches are discussed.
Fulltext Origin and diversity of an underutilized fruit tree crop, cempedak (Artocarpus integer, Moraceae)

Wang MMH, Gardner EM, Chung RCK, Chew MY, Milan AR, Pereira JT, et al.

Am J Bot, 2018 05;105(5):898-914.
PMID: 29874392 DOI: 10.1002/ajb2.1094

PREMISE OF THE STUDY: Underutilized crops and their wild relatives are important resources for crop improvement and food security. Cempedak [Artocarpus integer (Thunb). Merr.] is a significant crop in Malaysia but underutilized elsewhere. Here we performed molecular characterization of cempedak and its putative wild relative bangkong (Artocarpus integer (Thunb). Merr. var. silvestris Corner) to address questions regarding the origin and diversity of cempedak.
METHODS: Using data from 12 microsatellite loci, we assessed the genetic diversity and genetic/geographic structure for 353 cempedak and 175 bangkong accessions from Malaysia and neighboring countries and employed clonal analysis to characterize cempedak cultivars. We conducted haplotype network analyses on the trnH-psbA region in a subset of these samples. We also analyzed key vegetative characters that reportedly differentiate cempedak and bangkong.
KEY RESULTS: We show that cempedak and bangkong are sister taxa and distinct genetically and morphologically, but the directionality of domestication origin is unclear. Genetic diversity was generally higher in bangkong than in cempedak. We found a distinct genetic cluster for cempedak from Borneo as compared to cempedak from Peninsular Malaysia. Finally, cempedak cultivars with the same names did not always share the same genetic fingerprint.
CONCLUSIONS: Cempedak origins are complex, with likely admixture and hybridization with bangkong, warranting further investigation. We provide a baseline of genetic diversity of cempedak and bangkong in Malaysia and found that germplasm collections in Malaysia represent diverse coverage of the four cempedak genetic clusters detected.
Fulltext Paralogs and off-target sequences improve phylogenetic resolution in a densely-sampled study of the breadfruit genus (Artocarpus, Moraceae)

Gardner EM, Johnson MG, Pereira JT, Puad ASA, Arifiani D, Wickett NJ, et al.

Syst Biol, 2020 Sep 24;70(3):558-75.
PMID: 32970819 DOI: 10.1093/sysbio/syaa073

We present a 517-gene phylogenetic framework for the breadfruit genus Artocarpus (ca. 70 spp., Moraceae), making use of silica-dried leaves from recent fieldwork and herbarium specimens (some up to 106 years old) to achieve 96% taxon sampling. We explore issues relating to assembly, paralogous loci, partitions, and analysis method to reconstruct a phylogeny that is robust to variation in data and available tools. While codon partitioning did not result in any substantial topological differences, the inclusion of flanking non-coding sequence in analyses significantly increased the resolution of gene trees. We also found that increasing the size of datasets increased convergence between analysis methods but did not reduce gene tree conflict. We optimized the HybPiper targeted-enrichment sequence assembly pipeline for short sequences derived from degraded DNA extracted from museum specimens. While the subgenera of Artocarpus were monophyletic, revision is required at finer scales, particularly with respect to widespread species. We expect our results to provide a basis for further studies in Artocarpus and provide guidelines for future analyses of datasets based on target enrichment data, particularly those using sequences from both fresh and museum material, counseling careful attention to the potential of off-target sequences to improve resolution.
Fulltext Echoes of ancient introgression punctuate stable genomic lineages in the evolution of figs

Gardner EM, Bruun-Lund S, Niissalo M, Chantarasuwan B, Clement WL, Geri C, et al.

Proc Natl Acad Sci U S A, 2023 Jul 11;120(28):e2222035120.
PMID: 37399402 DOI: 10.1073/pnas.2222035120

Studies investigating the evolution of flowering plants have long focused on isolating mechanisms such as pollinator specificity. Some recent studies have proposed a role for introgressive hybridization between species, recognizing that isolating processes such as pollinator specialization may not be complete barriers to hybridization. Occasional hybridization may therefore lead to distinct yet reproductively connected lineages. We investigate the balance between introgression and reproductive isolation in a diverse clade using a densely sampled phylogenomic study of fig trees (Ficus, Moraceae). Codiversification with specialized pollinating wasps (Agaonidae) is recognized as a major engine of fig diversity, leading to about 850 species. Nevertheless, some studies have focused on the importance of hybridization in Ficus, highlighting the consequences of pollinator sharing. Here, we employ dense taxon sampling (520 species) throughout Moraceae and 1,751 loci to investigate phylogenetic relationships and the prevalence of introgression among species throughout the history of Ficus. We present a well-resolved phylogenomic backbone for Ficus, providing a solid foundation for an updated classification. Our results paint a picture of phylogenetically stable evolution within lineages punctuated by occasional local introgression events likely mediated by local pollinator sharing, illustrated by clear cases of cytoplasmic introgression that have been nearly drowned out of the nuclear genome through subsequent lineage fidelity. The phylogenetic history of figs thus highlights that while hybridization is an important process in plant evolution, the mere ability of species to hybridize locally does not necessarily translate into ongoing introgression between distant lineages, particularly in the presence of obligate plant-pollinator relationships.