Anatomy of a Neotropical insect radiation

Isaac Winkler,Luz Maria Huerto Santillan,Kristina J Ottens,Sonja J Scheffer,Andrew P Rasmussen,Marty A Condon,Matthew L Lewis,Géssica A Gomes-Costa,Andrew A Forbes

doi:10.1186/s12862-018-1146-9

Abstract

BackgroundMuch 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.ResultsThe 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.ConclusionsOverall 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.

Highlights

Much evolutionary theory predicts that diversity arises via both adaptive radiation and divergence of geographically isolated populations
How do ecology and geography interact to result in the origin of new animal diversity? From Darwin’s insight that both selection on ecological characters and geographic isolation generate species diversity [1], to Mayr’s [2] insistence that initiation of speciation occurs primarily in the context of geographic isolation, perspectives have shifted as to which factor deserves greater emphasis
Research on herbivorous insects has tended to emphasize the importance of ecology in driving speciation

Summary

Introduction

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. Studies of herbivorous insects in the incipient stages of speciation suggest a frequent role for ecological differentiation in driving the evolution of reproductive isolation (reviewed in [13,14,15]). These points have resulted in an emphasis on the importance of ecology, in the form of host shifts, for initiating divergence and driving species diversification [7, 13,14,15]. Though few would suggest that geographic isolation has played no role in herbivorous insect diversification, its importance in the literature on plant-insect evolution may have been under represented [19, 20]

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