Anatomy of a Neotropical Insect Radiation Isaac Winkler1*, Sonja J
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Winkler et al. BMC Evolutionary Biology (2018) 18:30 https://doi.org/10.1186/s12862-018-1146-9 RESEARCHARTICLE Open Access Anatomy of a Neotropical insect radiation Isaac Winkler1*, Sonja J. Scheffer2, Matthew L. Lewis2, Kristina J. Ottens3, Andrew P. Rasmussen1, Géssica A. Gomes-Costa4, Luz Maria Huerto Santillan5, Marty A. Condon1 and Andrew A. Forbes3 Abstract Background: Much evolutionary theory predicts that diversity arises via both adaptive radiation (diversification driven by selection against niche-overlap within communities) and divergence of geographically isolated populations. We focus on tropical fruit flies (Blepharoneura, Tephritidae) that reveal unexpected patterns of niche- overlap within local communities. Throughout the Neotropics, multiple sympatric non-interbreeding populations often share the same highly specialized patterns of host use (e.g., flies are specialists on flowers of a single gender of a single species of host plants). Lineage through time (LTT) plots can help distinguish patterns of diversification consistent with ecologically limited adaptive radiation from those predicted by ecologically neutral theories. Here, we use a time-calibrated phylogeny of Blepharoneura to test the hypothesis that patterns of Blepharoneura diversification are consistent with an “ecologically neutral” model of diversification that predicts that diversification is primarily a function of time and space. Results: The Blepharoneura phylogeny showed more cladogenic divergence associated with geography than with shifts in host-use. Shifts in host-use were associated with ~ 20% of recent splits (< 3 Ma), but > 60% of older splits (> 3 Ma). In the overall tree, gamma statistic and maximum likelihood model fitting showed no evidence of diversification rate changes though there was a weak signature of slowing diversification rate in one of the component clades. Conclusions: Overall patterns of Blepharoneura diversity are inconsistent with a traditional explanation of adaptive radiation involving decreases in diversification rates associated with niche-overlap. Sister lineages usually use the same host-species and host-parts, and multiple non-interbreeding sympatric populations regularly co-occur on the same hosts. We suggest that most lineage origins (phylogenetic splits) occur in allopatry, usually without shifts in host-use, and that subsequent dispersal results in assembly of communities composed of multiple sympatric non-interbreeding populations of flies that share the same hosts. Keywords: Speciation, Lineage through time (LTT) plots, Neutral theory, Diversification, Host-use, Tropics, Herbivorous insects, Parasitoids Background ecology: abiotic factors (soil type, elevation, climate, etc.) How do ecology and geography interact to result in the vary over geographic space, and distant sites may differ (or origin of new animal diversity? From Darwin’s insight not) in their environments. Geographic isolation may that both selection on ecological characters and geo- therefore result in the accumulation of reproductive isola- graphic isolation generate species diversity [1], to Mayr’s tion due to a combination of factors: stochastic change [2] insistence that initiation of speciation occurs primarily (e.g., drift), selection in different ecological environments, in the context of geographic isolation, perspectives have and sexual selection that can result in divergent patterns shifted as to which factor deserves greater emphasis. Yet, of courtship. As individuals from geographically isolated current researchers (e.g. [3, 4]) acknowledge that the roles populations move through time and space, secondary of ecology and geographic isolation are complementary contact between previously isolated, divergent populations and obligatorily intertwined. Geography, after all, affects can allow for ecological interaction between incipient lineages and/or reinforcement of reproductive barriers [5] * Correspondence: [email protected] both of which could result in further evolution of eco- 1Department of Biology, Cornell College, Mount Vernon, Iowa 52314, USA Full list of author information is available at the end of the article logically relevant characters [6]. © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Winkler et al. BMC Evolutionary Biology (2018) 18:30 Page 2 of 13 Exceptions to this synthetic view may often be found plant. We discovered an even more diverse community among the expansive literature on the evolution of herb- along a 1 km transect in Peru: we reared fifteen species of ivorous insects, a group of animals representing at least Blepharoneura from flowers of just two host plant species: a quarter of macroscopic species [7]. For several reasons, G. acuminata and G. spinulosa [23], and more recent research on herbivorous insects has tended to emphasize work suggests this may have been an underestimate the importance of ecology in driving speciation. First, of total diversity [24]. Such high levels of niche over- herbivory is a key innovation that has consistently lap [22–24] are not predicted by classic models of resulted in increased diversification across insect taxa adaptive radiation [25, 26]. [8, 9]. Second, phylogenies of herbivorous insect lineages In Blepharoneura communities, direct competition for often show a pattern indicative of adaptive radiation: di- host resources is unlikely: we consistently find that fewer versification correlates with entry into successive, often than a third of flowers are occupied by larvae [23]. nested adaptive zones defined by plant chemistry and tax- Furthermore, the current phylogeny shows [21] that onomy [10–12]. Third, studies of herbivorous insects in many divergence events are not accompanied by host the incipient stages of speciation suggest a frequent role shifts. Those patterns, and the observation that multiple for ecological differentiation in driving the evolution of re- sympatric species occupy the same feeding-niche appar- productive isolation (reviewed in [13–15]). These points ently without competing, led us to suggest that diversifi- have resulted in an emphasis on the importance of cation of Blepharoneura appeared to be ecologically ecology, specifically in the form of host shifts, for initiating neutral [21]. Yet, selective pressures associated with divergence and driving species diversification [7, 13–15]. host-use are not only associated with competition for Host shifts are thought to promote diversification when food resources. Parasitoids can impose strong selection courtship and mating are restricted to the host (thus on patterns of host-use by herbivores [17, 18, 27, 28]: restricting gene flow between host-specific populations) many parasitoids find and attack their hosts only on one [16] and when host-specific predators select for shifts species of plant; herbivores on alternate hosts escape to “enemy-free space” [17, 18]. Though few would death. Blepharoneura are attacked by host-specific para- suggest that geographic isolation has played no role sitoid wasps in the opiine subgenus Bellopius (Braconi- in herbivorous insect diversification, its importance in dae): each species of Bellopius attacks flies in a single the literature on plant-insect evolution may have been host-plant species and sex-flower, and can kill only one under represented [19, 20]. species of Blepharoneura[23]. These lethal wasps show Our interest in the causes of herbivorous insect greater fidelity to host plant species than even their host speciation stems from our ongoing, intensive study of a flies do, and thus could exert significant selection for tropical herbivore radiation: a diverse group of cryptic shifts to alternate host plants (e.g. [29, 30]). species in the genus Blepharoneura (Tephritidae). These Lineage-through-time (LTT) plots have been used true fruit flies, found across tropical America, all feed on to identify patterns consistent with adaptive radiation plants in the Cucurbitaceae (the squash and melon [31–33]. For instance, a classic signature of adaptive family), and almost all are specialists on specific plant radiation is an initial increase in diversification rate, parts (e.g., male versus female flowers, seeds, or stems) followed by a decrease in diversification rate towards of single species of cucurbits. An especially diverse the present (negative gamma values) [25, 26, 32, 34]. group of Blepharoneura specializes on highly sexually This expectation is based on the widely held assump- dimorphic plants in the subtribe Guraniinae (Gurania tion that speciation and extinction rates are strongly and its close relative, Psiguria). Previous phylogenetic dependent on the number of available, unoccupied study [21] revealed ancient colonization of major cucur- niches [26]. Alternatively, ecologically neutral diversi- bit clades (tribes and subtribes), followed by diversifica- fication can result in two types of LTT plots. LTT tion of specialists, often without shifts in host-use. plots with slower initial