Out of Borneo: biogeography, phylogeny and divergence date estimates ofArtocarpus(Moraceae)

Abstract

Background and Aims The breadfruit genus (Artocarpus, Moraceae) includes valuable underutilized fruit tree crops with a centre of diversity in Southeast Asia. It belongs to the monophyletic tribe Artocarpeae, whose only other members include two small neotropical genera. This study aimed to reconstruct the phylogeny, estimate divergence dates and infer ancestral ranges of Artocarpeae, especially Artocarpus, to better understand spatial and temporal evolutionary relationships and dispersal patterns in a geologically complex region.Methods To investigate the phylogeny and biogeography of Artocarpeae, this study used Bayesian and maximum likelihood approaches to analyze DNA sequences from six plastid and two nuclear regions from 75% of Artocarpus species, both neotropical Artocarpeae genera, and members of all other Moraceae tribes. Six fossil-based calibrations within the Moraceae family were used to infer divergence times. Ancestral areas and estimated dispersal events were also inferred.Key Results Artocarpeae, Artocarpus and four monophyletic Artocarpus subgenera were well supported. A late Cretaceous origin of the Artocarpeae tribe in the Americas is inferred, followed by Eocene radiation of Artocarpus in Asia, with the greatest diversification occurring during the Miocene. Borneo is reconstructed as the ancestral range of Artocarpus, with dozens of independent in situ diversification events inferred there, as well as dispersal events to other regions of Southeast Asia. Dispersal pathways of Artocarpus and its ancestors are proposed.Conclusions Borneo was central in the diversification of the genus Artocarpus and probably served as the centre from which species dispersed and diversified in several directions. The greatest amount of diversification is inferred to have occurred during the Miocene, when sea levels fluctuated and land connections frequently existed between Borneo, mainland Asia, Sumatra and Java. Many species found in these areas have extant overlapping ranges, suggesting that sympatric speciation may have occurred. By contrast, Artocarpus diversity east of Borneo (where many of the islands have no historical connections to the landmasses of the Sunda and Sahul shelves) is unique and probably the product of over water long-distance dispersal events and subsequent diversification in allopatry. This work represents the most comprehensive Artocarpus phylogeny and biogeography study to date and supports Borneo as an evolutionary biodiversity hotspot.

Which frugivory‐related traits facilitated historical long‐distance dispersal in the custard apple family (Annonaceae)?

“…Since Humboldt's travels (e.g., 1889), an important finding in the field of historical biogeography has been that long‐distance dispersal (vs. vicariance) may have been the rule rather than the exception to explain the pantropical distribution of many plant families (e.g., Myristicaceae, Doyle et al., ; Melastomataceae, Renner, 2004b; Monimiaceae, Renner et al., ; Arecaceae, Baker & Couvreur, ; Moraceae, Williams et al., ). Nevertheless, it has remained puzzling by which mechanism these long‐distance dispersal events have occurred (Morley, ; Thorne, ; van Steenis, ).…”

“…Indeed, palms likely also possessed megafaunal fruits during their Late Cretaceous/ Early Cenozoic dispersals across Africa, Asia and South America (Baker & Couvreur, 2013;Onstein et al, 2018). Furthermore, Asian elephants (Elephas maximus) and their ancestors were proposed as important seed dispersers of several of the megafaunal-fruited Artocarpus (Moraceae) species in South-East Asia (Williams et al, 2017). Many megafaunal seed dispersers, such as South American proboscideans, xenarthrans and Notoungulata, went extinct in the Late Quaternary (Barnosky, Koch, Feranec, Wing, & Shabel, 2004), and present-day plants with megafaunal fruits therefore suffer from dispersal limitation, small geographical ranges, and, possibly, extinction (Guimarães et al, 2008;Onstein et al, 2018;Pires et al, 2017).…”

In the footsteps of Wallace: population structure in the breadfruit fruit fly, Bactrocera umbrosa (F.) (Diptera: Tephritidae), suggests disjunction across the Indo‐Australian Archipelago

“…Jackfruit is thought to be native to the Western Ghats (India), although alternate hypotheses for its origins exist, including Malaysia (Zielenski 1955;Barrau 1976) and Bangladesh (Khan et al 2010). In contrast, the breadfruit complex is native to islands east of these Lines, following earlier divergence from a Bornean ancestor (Williams et al 2017). In contrast, the breadfruit complex is native to islands east of these Lines, following earlier divergence from a Bornean ancestor (Williams et al 2017).…”

“…In contrast, the breadfruit complex is native to islands east of these Lines, following earlier divergence from a Bornean ancestor (Williams et al 2017). It is plausible, therefore, that B. umbrosa originated in the West Pacific (possibly on New Guinea), where it utilised either a now-extinct Artocarpus species or an ancestor of breadfruit (Williams et al 2017). Additionally, anecdotal evidence also suggests behavioural differences in host use.…”

“…This species has a native distribution that ranges from mainland Thailand through the archipelago, to the Philippines and to the West Pacific islands of New Caledonia and Vanuatu (Drew 1989;Drew & Romig 2013). communis) (Jarrett 1959;Berg et al 2006), it is now recognised that they represent distinct species (Zerega et al 2005;Zerega et al 2010;Williams et al 2017). The host range of B. umbrosa is restricted to a small number of Artocarpus species, specifically, Artocarpus integer (chempedak), A. heterophyllus (jackfruit) and A. altilis (breadfruit) (Allwood et al 1999;Leblanc et al 2013).…”