Biogeography

We used Artocarpus species distribution information from Jarrett (1959a, b, c, 1960, 1975), Kochummen (2000), Soepadmo and Saw (2000), Berg (2001, 2005), Zhekun and Gilbert (2003) and Berg et al. (2006, 2011) to assign Artocarpus taxa to the following areas, modified from Turner et al. (2001): Southern China, Western Ghats of India, Indo-Burma sensu Myers et al. (2000), Thai-Malay Peninsula, Borneo, Sumatra, Java, Philippines, Sulawesi and east of Sulawesi (Table 1). For other Artocarpeae and outgroup taxa we included Africa, Eurasia, North/Central America, and South America. For taxa found in more than one area, multiple assignments were allowed, with six areas being the highest for a single taxon. To reconstruct ancestral ranges and estimate dispersal events we used S-DIVA (Yu et al., 2010) and Lagrange (Ree and Smith, 2008) as implemented in RASP v.3.02 (Yu et al., 2015) using the single-accession exemplar dataset. In S-DIVA, we used 201 Beast output trees to test two to four areas per node with and without extinction, and no constraints on dispersal. In Lagrange we tested two to three areas per node, with and without dispersal constraints. Dispersal constraints followed those in Webb and Ree (2012), which we coded with the probability of 0·5 to allow dispersals between all areas. To visualize dispersal, the number and direction of dispersal events were calculated based on the most likely (>50%) ancestral range reconstructions at each node. In cases where the most likely range reconstruction consisted of two areas, all permutations of dispersal were assigned with a value that was proportional such that each node was only counted once. For example, if a dispersal event was reconstructed from a node with one area (X) to a node with two areas (YZ), then X to Y was assigned a value of 0·5, and X to Z was assigned a value of 0·5.

Biogeography

Analyses using Lagrange and SDIVA produced similar results (Supplementary Data Table S3, Fig. S2), with strong support for Borneo as the ancestral range for Artocarpus (Fig. 3). The results presented here are based on allowing two ancestral regions per node and no dispersal constraints. The root of the tribe Artocarpeae is reconstructed as North/Central America and South America. Range reconstruction of Artocarpus inferred the most cases of in situ diversification in Borneo (42 events) followed by the Thai Malay peninsula (eight events), the Philippines (six events) and East of Sulawesi (five events) (Fig. 4, Supplementary Data Table S4). Borneo was inferred as the source of the most dispersal events (32 events), followed by the Thai-Malay Peninsula (12 events) (Fig. 4, Table S4). Dispersal events from Borneo include movement eastward across Wallace’s line (i.e. A. fretessii), westward into the Thai-Malay Peninsula (i.e. A. lanceifolius), northward into Indo-Burma (A. dadah Miq.) and north-east into the Philippines (A. odoratissimus Blanco).

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Fig. 4.

Dispersal and in situ speciation events in Artocarpus. Arrows indicate dispersal events, and are colour-coded to match the region from which the event originated. Line thickness is proportional to the number of events. The circled numbers in each area indicate the number of in situ diversification events in that region. Events with an occurrence of 1·0 or higher are displayed. See Table S4 for all events.

Dating and biogeography

In the mid- to late Cretaceous (83·8 Mya, 74·85–92·65 Mya) the stem node of the tribe Artocarpeae diverged from the rest of the family Moraceae. The biogeographical reconstruction infers a likely origin of the tribe in the Americas. The split between American (Clarisia and Batocarpus) and Asian Artocarpeae (Artocarpus) occurred in the Palaeocene (59·67 Mya, 55·24–65·03 Mya) with a radiation of Artocarpus from Borneo in the Eocene to Oligocene (40·07 Mya, 29·8–50·81 Mya). The time frame in which Artocarpus radiated coincides with boreotropical flora and a North Atlantic Land Bridge that could have allowed for dispersal from the Americas into Eurasia (McLoughlin, 2001). We are unaware of any fossil evidence for Batocarpus and Clarisia, but there are several records of fossils of Artocarpus and related extinct taxa (Artocarpoxylon, Artocarpoxidium and Artocarpoides) in Austria, France, Texas, Colorado, Louisiana, Canada, Kansas and Greenland from the Cretaceous into the Eocene (Collinson, 1989). These fossils support the possible presence of Artocarpus ancestors in areas where they might be expected if there had been dispersal across a North Atlantic Land Bridge. However, they must be viewed with some caution, and this is why they were not used in divergence date estimates. The vast majority of the fossils are from deeply cleft fossil leaves, which share gross similarities with some extant Artocarpus species, but the fossils lack cuticles and have poorly preserved venation. In her review of Moraceae fossils, Collinson (1989) indicated that these leaf fossils may be correctly identified as Artocarpus ancestors, but they are not 100% diagnostic. In summary, the data presented here suggest an ancestral range for Artocarpeae in the Americas and dispersal across a North Atlantic Land Bridge in the Eocene during a time of boreotropical flora. Further detailed examination of fossil data is warranted to determine how well they support this proposal.

Artocarpus ancestors probably spread throughout Eurasia in the Eocene and began to diversify during this period of higher global temperatures. There are limited fossils of Artocarpus and its ancestors in Asia, but there are well-characterized wood fossils from the Intertrappean Deccan Beds in India dated from the Palaeocene to the Miocene periods, suggesting the genus or its ancestors had reached India by then (Mehrotra et al., 1984). This is consistent with dispersal across land, as India collided with Asia sometime between 43 and 50 Mya (McLoughlin, 2001; Sanmartín and Ronquist, 2004). Also, the first ever Artocarpus fossil from China was recently described from a site that is considered to have strong phytogeographical connections with India (Jacques et al., 2015). The fossil is well preserved and comes from the middle Miocene Fotan flora of Zhangpu County, South Fujian, China, an area that has been considered to represent tropical rainforest based on the occurrence of distinctive winged fruit fossils (Jacques et al., 2015).

From southern Asia Artocarpus could have dispersed across land into what is now the island of Borneo. While Artocarpus may ultimately derive from extinct taxa in mainland Asia, Borneo is reconstructed as the greatest incubator of extant diversity and the ancestral range of Artocarpus as it exists today. Diversification in Borneo may have been followed by several separate dispersal events (and subsequent radiations) throughout Southeast Asia and Malesia (Figs 3 and 4). Radiation of Artocarpus is reconstructed as beginning in the Eocene and continuing through the Oligocene and into the Miocene and Pliocene, with the greatest diversification inferred to occur in the Miocene. Fluctuating sea levels during these periods may have allowed for isolation and diversification during times of high sea levels, followed by radiation and dispersal during periods of lower sea levels (Turner et al., 2001). During the Miocene, sea levels were generally lower than they are today, and frequent land connections existed between mainland Asia, the Thai/Malay peninsula and what is now northern and central Borneo, and parts of Sumatra and western Java (Hall, 2009, 2012; de Bruyn et al., 2014). However, the Philippines, Sulawesi, the Moluccas and other islands of Wallacea were frequently submerged until the mid-Miocene to Pliocene and did not share land connections to Borneo or to each other.

Considering the extant range for Artocarpus species included in this study, Borneo experienced higher levels of in situ diversification and emigration than any other area, especially during the Miocene. Borneo, the Thai-Malay Peninsula, mainland Asia, and parts of Sumatra and Java were frequently connected between 60 and 5 Mya (Hall, 2009; de Bruyn et al., 2014), and the species found in these areas have largely overlapping ranges today, suggesting that sympatric speciation may have occurred followed by dispersal (Fig. 4). The Thai-Malay Peninsula may have been a gateway for Artocarpus from Borneo into mainland Asia, Sumatra and Java. For example, half of the Thai-Malay taxa included in the study diversified in Borneo. All of the Artocarpus taxa in Java and Sumatra are a subset of what is found in the Thai-Malay Peninsula. Sumatra was connected to the Thai-Malay Peninsula and parts of Borneo (but closer to the former) from the Palaeocene into the Oligocene, and variously connected and disconnected due to fluctuating water levels in the Miocene. Several of the species in Sumatra are not found in Borneo and are only otherwise known from the Thai-Malay Peninsula. This, along with ancestral range reconstructions, suggests that dispersal into Sumatra came through the Thai-Malay Peninsula (Fig. 3). Java in turn houses a subset of the Sumatran taxa, suggesting taxa dispersed into Java from Sumatra, probably during the late Miocene and early Pliocene when dispersal would have been more likely. Moving northward, based on the taxa in this study, Indo-Burma houses 73% of the taxa found in the Thai-Malay Peninsula (but only 40% of Borneo taxa), and southern China in turn houses 83% of the taxa found in Indo-Burma (but only 33% of Thai-Malay Peninsula and 0% of Borneo taxa) (Table S1). This suggests northward dispersal of taxa out of Borneo into the Thai-Malay Peninsula, Indo-Burma and southern China, with some in situ diversification of new species throughout the Miocene and into the Pliocene (Figs 3 and 4). An alternative, and not mutually exclusive, explanation is allopatric speciation on the variously isolated landmasses during times of sea-level fluctuations with secondary contact after dispersal to Borneo. Possible dispersal routes over water are discussed below.

An outlier in Artocarpus distribution is the Western Ghats of southern India. An Indo-Malayan influence in the flora and fauna of southern India has long been recognized (Hora, 1944, 1949), and there are many examples of extant plant taxa present in the wet tropical forests of the Western Ghats and north-eastern India, but absent from the more arid central Indian region (Bahulikar et al., 2004; Apte et al., 2006; Banu et al., 2009; Kuttapetty et al., 2014). Recent analysis of fossil flora from the Deccan Intertrappean beds in central India suggests that the wet tropical forests, similar to present-day forests of the Western Ghats and north-east India, were flourishing in central India during the late Cretaceous into the Oligocene (Kapgate, 2013). Artocarpus hirsutus is restricted to the Western Ghats and it is reconstructed with an ancestral area of Borneo. Its extant distribution may be the result of long-distance overwater dispersal from Borneo to the Indian peninsula, or it may be the result of overland dispersal of its ancestral lineage through the Thai-Malay Peninsula into the Asian mainland and into India during a period when central India would have been home to wet tropical forests, but it has subsequently gone extinct outside of the Western Ghats (Figs 3 and 4). Given that support for its position in the phylogeny is low and it has been considered a morphologically anomalous species difficult to place (Jarrett, 1959a, b, c; Zerega et al., 2010), further work is needed to elucidate the evolutionary and biogeographical history of this species. Another Western Ghats species (A. heterophyllus, jackfruit) is a complicated taxon, as it is an economically important crop that is widely cultivated throughout the tropics today. It exhibits high levels of morphological (Azad et al., 2007; Khan et al., 2010) and genetic diversity (Melhem, 2015) in the Western Ghats, and this area has been proposed as its area of origin. However, high levels of morphological and genetic diversity also exist in Indo-Burma (Bangladesh) (Khan et al., 2010; Witherup, 2013; Witherup et al., 2013), and its centre of diversity and wild relative(s) remain unclear. Given that it may also be native in Indo-Burma and that its sister species, A. integer (cempedak, an important crop in Malaysia), is native to the Thai-Malay Peninsula and Borneo, A. heterophyllus may have reached the Western Ghats via overland dispersal through Indo-Burma. Inclusion of the Sri Lankan endemic, A. nobilis Thwaites, in future phylogenetic analyses, as well as phylogeographical studies of Western Ghats species such as A. heterophyllus and A. hirsutus, could help further elucidate biogeographical patterns in Artocarpus between Indo-Malaya and India.

Apart from one very widely distributed taxon (A. teijsmannii), Sulawesi and islands eastwards harbour very different species diversity than mainland Asia, Sumatra and Java, but they share diversity with Borneo. Sulawesi taxa are largely a subset of Borneo taxa, and our results infer a dispersal event to Sulawesi from Borneo during the Miocene (Table S4). Taxa present eastward, in Wallacea and Oceania, are the same as those in Sulawesi plus three additional lineages that may have diversified in New Guinea and Oceania [A. papuanus (Becc.) Renner, A. sepicanus Diels, and the lineage containing A. altilis, A. camansi Blanco and A. mariannensis Trécul – breadfruit and its wild progenitors]. Because there were no land connections from Borneo into Sulawesi and Wallacea, this finding suggests overwater dispersal from Borneo, mostly during the Miocene. The Artocarpus taxa on the islands of the Philippines are quite distinct. Of the Philippine taxa included in this study, only 29% of them have distributions overlapping with Borneo and there is no overlap with any other region apart from the widespread A. sericicarpus Jarrett. The Philippines is home to a high number of endemic taxa that diversified in the mid-Miocene to Pliocene, when the Philippine islands became emergent (Hall, 1998). There are additional endemic Philippine Artocarpus taxa that we were unable to include in the present study. They have morphological affinities to taxa included in the present study, suggesting that once taxa reached the islands, in situ species radiation was not uncommon.

With several inferred dispersal events across large expanses of water from Borneo into Sulawesi and eastward (Fig. 4, Table S4), it is important to consider how these may have occurred. Dispersal of syncarps and seeds in Artocarpus is not well studied. Large syncarps often drop and germinate near the mother tree (N. J. C. Zerega, pers. observ.) or are consumed by large mammals, such as elephants, orangutans and flying foxes (Campbell-Smith et al., 2011; Canale et al., 2013; Sekar et al., 2015; Sekar and Sukumar, 2015). However, whether the seeds survive passage through mammalian guts or if such passage increases germination rates is largely unknown. Recent studies examined whether Asian tapirs could facilitate long-distance seed dispersal in several species including A. integer (Thunb.) Merr. (Campos-Arceiz et al., 2012). They found that the tapirs consumed very few seeds, and of those that were consumed only 2·8% of A. integer seeds survived passage through the gut and 0% were able to germinate (Campos-Arceiz et al., 2012). Sekar et al. (2015) tested how well domestic bovids (Bos primigenius – cattle, and Bubalus bubalis – buffalo) and Asian elephants (Elephas maximus) in India could disperse A. chama seeds. They found that seeds passing through elephants are more likely to survive and germinate compared to seeds passing through bovids, and that elephants can act as dispersers of A. chama seeds. The ancestors of modern Asian elephants diverged from mastodons in the Oligocene and diverged from the African elephant (Loxodonta africana) in the late Miocene (Kappelman et al., 2003; Shoshani et al., 2006; Rohland et al., 2007). Asian elephants and their ancestors may have been important dispersers of several Artocarpus species (Sekar et al., 2015). This mode of dispersal may help to explain the expansion of Artocarpus from Borneo throughout parts of mainland Asia. As the range of the modern Asian elephant and other large mammals shrinks, so too may the dispersal of Artocarpus species.

With regard to dispersal across long distances of open water to the islands east of Borneo, a possible disperser may have been flying foxes (Pteropus ssp.). Much of the diversification within Pteropus occurred in the Miocene to Pliocene, coinciding with Artocarpus diversification (Almeida et al., 2014). Various Artocarpus species have been recorded as preferred roosting sites and a food source for several Pteropus species in the Caroline Islands, Philippines and elsewhere (Mildenstein et al., 2005; Buden et al., 2013). Pteropus species are predominantly insular species with restricted ranges and are capable of flying up to 50km in a single night (Mickleburgh et al., 1992; Almeida et al., 2014). There is a great deal of diversity and endemism of Pteropus species, which can be explained by its being a specialized island taxon. Islands provide isolated areas (allopatry) where divergence can proceed relatively quickly by genetic drift without interference from frequent gene flow. Sympatry of Pteropus species most often results from multiple colonization events rather than in situ speciation (Almeida et al., 2014). This same pattern is observed in Artocarpus species in the islands east of Borneo; however, in situ diversification is also important (Fig. 4, Table S4). Further investigation of the ecological interactions between Artocarpus and Pteropus is warranted.