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

Abstract

Understanding the interplay between plant host and insect herbivore diversification underpins many areas of pure and applied research. The tephritid fruit fly Bactrocera umbrosa is a primary pest of a small number of Artocarpus species throughout Southeast Asia and the West Pacific. Recent molecular evidence supports a pattern of eastward migration and species diversification in Artocarpus. Here, we aimed to test whether population structure in B. umbrosa was associated with historical biogeographical barriers such as Wallace's Line and discuss observed patterns in the context of Artocarpus diversification. We used an integrative approach to explore population structure within B. umbrosa based on morphological (wing shape and aedeagus length) and molecular (mitochondrial COI and COII) data. Overall, aedeagi and wing centroid sizes were generally larger and exhibited greater variation in the West Pacific than Southeast Asia. Molecular data agreed with this trend, and COI also showed a subtle but clear disjunction between regions associated with Weber/Lydekker's Lines. Taken together, the West Pacific was supported as the putative origin of B. umbrosa, whereas movement westward into Southeast Asia occurred more recently, likely via a single colonisation event followed by highly restricted gene flow. Population structure in B. umbrosa does not reflect an ancient history of tracking Artocarpus diversification eastward out of Southeast Asia.

The Dacini fruit fly fauna of Sulawesi fits Lydekker’s line but also supports Wallacea as a biogeographic region (Diptera, Tephritidae)

“…This is in stark contrast with affinities related to Sahul; only one species is currently also found there, and an additional single species is found across Sunda, Wallacea and Sahul ( B. umbrosa (Fabricius, 1805); see also Krosch et al 2018 ). All 47 other species are endemic to Wallacea, and 39 of those are known from Sulawesi only, indicating the high levels of endemicity of the region, even for these volant insects.…”

“…We further encountered small numbers of B. umbrosa , a pest of breadfruit ( Artocarpus altilis ) that has an extraordinarily wide distribution; it is the only species in the checklist that is known to be naturally dispersed across Southeast Asia, Wallacea, Australia and Oceania ( Krosch et al 2018 ). We suggest that, if desired, the population densities of pests in our survey areas can likely be decreased significantly with sanitation measures, most importantly the removal of fallen fruit and pruning of damaged fruit unfit for consumption.…”

“…It has been advocated by some that the categorization of biogeographic regions should follow more quantitative measures (Kreft and Jetz 2010), as opposed to the qualitative assessments from the early explorers. Using a non-metric multidimensional scaling approach across a wide range of taxa, Kreft and Jetz (2010) suggested that Lydekker's line was most appropriate for separating the Oriental region from Australasia. This agrees with our findings for Dacini, although, depending on the scale of the patterns in question, maintaining Wallacea as a separate biogeographic region can equally well be argued.…”

“…Biogeographic boundaries were initially established to indicate stark and sudden differences between faunas of neighboring areas, as noted by early explorers like Alfred Russel Wallace, and proved fundamental to the understanding of tectonic plate movement (Wallace 1876;Lydekker 1896;Mayr 1944;Simpson 1977;Whitmore 1982). Today, they incorporate phylogenetic considerations and define biogeographical regions that can be of broad practical use including for regional identification keys, for understanding dispersal patterns, and designation of biogeographic hotspots for critical conservation considerations (Kreft and Jetz 2010;van Welzen et al 2011;Holt et al 2013). The area that connects Southeast Asia with Australia -also termed the Malay Archipelago or Malesia -probably contains the largest number of named biogeographic boundaries anywhere on the planet (Simpson 1977).…”

Divergent east-west lineages in an Australian fruit fly associated with the Carpentaria basin divide

“…Population genetics seeks to understand population structuring and divergence within a species and is thus another tool for untangling the drivers of initial divergence within Bactrocera species. Population structuring in tephritid species is generally weak (11, 12), but nevertheless population-level divergence within tephritid species has been linked with differential host use (13, 14), increasing geographic distance (15, 16), and gene flow restriction associated with biogeographic barriers (17, 18). Within Australia, population genetic studies have only been applied to the pest B. tryoni , with the general pattern of findings for this species being little or no genetic structuring across the vast distribution (>2000km) of the endemic east coast population, but with structuring from east to west across Australia’s tropical ‘Top End’ (19–22).…”