Rapid radiation of ant parasitic butterflies during the Miocene aridification of Africa

Abstract Africa has undergone a progressive aridification during the last 20 My that presumably impacted organisms and fostered the evolution of life history adaptations. We test the hypothesis that shift to living in ant nests and feeding on ant brood by larvae of phyto‐predaceous Lepidochrysops butterflies was an adaptive response to the aridification of Africa that facilitated the subsequent radiation of butterflies in this genus. Using anchored hybrid enrichment we constructed a time‐calibrated phylogeny for Lepidochrysops and its closest, non‐parasitic relatives in the Euchrysops section (Poloyommatini). We estimated ancestral areas across the phylogeny with process‐based biogeographical models and diversification rates relying on time‐variable and clade‐heterogeneous birth‐death models. The Euchrysops section originated with the emerging Miombo woodlands about 22 million years ago (Mya) and spread to drier biomes as they became available in the late Miocene. The diversification of the non‐parasitic lineages decreased as aridification intensified around 10 Mya, culminating in diversity decline. In contrast, the diversification of the phyto‐predaceous Lepidochrysops lineage proceeded rapidly from about 6.5 Mya when this unusual life history likely first evolved. The Miombo woodlands were the cradle for diversification of the Euchrysops section, and our findings are consistent with the hypothesis that aridification during the Miocene selected for a phyto‐predaceous life history in species of Lepidochrysops, with ant nests likely providing caterpillars a safe refuge from fire and a source of food when vegetation was scarce.

[1]  A. Armstrong,et al.  Article continued - Outcomes of the Southern African Lepidoptera Conservation Assessment (SALCA) , 2022, Metamorphosis.

[2]  David J. Lohman,et al.  Miocene Climate and Habitat Change Drove Diversification in Bicyclus, Africa’s Largest Radiation of Satyrine Butterflies , 2021, Systematic biology.

[3]  R. Vilà,et al.  Explosive Radiation of Ant Parasitic Butterflies During the Miocene Aridification of Africa , 2021 .

[4]  B. O. Wolf,et al.  Exposure to climate change drives stability or collapse of desert mammal and bird communities , 2021, Science.

[5]  Andrew J. Helmstetter,et al.  Pulled Diversification Rates, Lineages-Through-Time Plots, and Modern Macroevolutionary Modeling , 2021, bioRxiv.

[6]  N. Pierce,et al.  Recent diversification of Chrysoritis butterflies in the South African Cape (Lepidoptera: Lycaenidae). , 2020, Molecular phylogenetics and evolution.

[7]  Matthew W. Pennell,et al.  Extant timetrees are consistent with a myriad of diversification histories , 2020, Nature.

[8]  A. Lemmon,et al.  Hierarchical Hybrid Enrichment: Multitiered Genomic Data Collection Across Evolutionary Scales, With Application to Chorus Frogs (Pseudacris) , 2019, Systematic biology.

[9]  P. Brakefield,et al.  To mate, or not to mate: The evolution of reproductive diapause facilitates insect radiation into African savannahs in the Late Miocene , 2019, bioRxiv.

[10]  Maryam Rabiee,et al.  Multi-allele species reconstruction using ASTRAL , 2018, bioRxiv.

[11]  Emmanuel F. A. Toussaint,et al.  Opposite macroevolutionary responses to environmental changes in grasses and insects during the Neogene grassland expansion , 2018, Nature Communications.

[12]  R. Vilà,et al.  Ecological specialization is associated with genetic structure in the ant-associated butterfly family Lycaenidae , 2018, Proceedings of the Royal Society B: Biological Sciences.

[13]  David J. Lohman,et al.  Evolution of Hypolimnas butterflies (Nymphalidae): Out-of-Africa origin and Wolbachia-mediated introgression. , 2018, Molecular phylogenetics and evolution.

[14]  M. Suchard,et al.  Posterior Summarization in Bayesian Phylogenetics Using Tracer 1.7 , 2018, Systematic biology.

[15]  Gerard Talavera,et al.  A Comprehensive and Dated Phylogenomic Analysis of Butterflies , 2018, Current Biology.

[16]  N. Wahlberg,et al.  Priors and Posteriors in Bayesian Timing of Divergence Analyses: The Age of Butterflies Revisited , 2019, Systematic biology.

[17]  Chao Zhang,et al.  ASTRAL-III: Increased Scalability and Impacts of Contracting Low Support Branches , 2017, RECOMB-CG.

[18]  N. Alvarez,et al.  High Rate of Protein Coding Sequence Evolution and Species Diversification in the Lycaenids , 2017, Front. Ecol. Evol..

[19]  A. von Haeseler,et al.  UFBoot2: Improving the Ultrafast Bootstrap Approximation , 2017, bioRxiv.

[20]  Jonas Eberle,et al.  Landscape genetics indicate recently increased habitat fragmentation in African forest‐associated chafers , 2017, Global change biology.

[21]  Thomas K. F. Wong,et al.  ModelFinder: Fast Model Selection for Accurate Phylogenetic Estimates , 2017, Nature Methods.

[22]  Neil D. Burgess,et al.  An Ecoregion-Based Approach to Protecting Half the Terrestrial Realm , 2017, Bioscience.

[23]  A. Ellis,et al.  Evolutionary history of a keystone pollinator parallels the biome occupancy of angiosperms in the Greater Cape Floristic Region. , 2017, Molecular phylogenetics and evolution.

[24]  T. Herbert,et al.  Late Miocene global cooling and the rise of modern ecosystems , 2016 .

[25]  A. Lemmon,et al.  Expanding anchored hybrid enrichment to resolve both deep and shallow relationships within the spider tree of life , 2016, BMC Evolutionary Biology.

[26]  M. Elgar,et al.  Eavesdropping on cooperative communication within an ant-butterfly mutualism , 2016, The Science of Nature.

[27]  M. R. May,et al.  A Bayesian approach for detecting the impact of mass‐extinction events on molecular phylogenies when rates of lineage diversification may vary , 2016 .

[28]  A. Lemmon,et al.  Integrating phylogenomic and morphological data to assess candidate species‐delimitation models in brown and red‐bellied snakes (Storeria) , 2016 .

[29]  Hélène Morlon,et al.  RPANDA: an R package for macroevolutionary analyses on phylogenetic trees , 2016 .

[30]  Sebastian Höhna,et al.  TESS: an R package for efficiently simulating phylogenetic trees and performing Bayesian inference of lineage diversification rates , 2016, Bioinform..

[31]  Champak R. Beeravolu,et al.  An Extended Maximum Likelihood Inference of Geographic Range Evolution by Dispersal, Local Extinction and Cladogenesis , 2016, bioRxiv.

[32]  Marek L Borowiec,et al.  AMAS: a fast tool for alignment manipulation and computing of summary statistics , 2016, PeerJ.

[33]  Siavash Mirarab,et al.  Fast Coalescent-Based Computation of Local Branch Support from Quartet Frequencies , 2016, Molecular biology and evolution.

[34]  J. Townsend,et al.  A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing , 2015, Nature.

[35]  B. O’Meara,et al.  Extinction can be estimated from moderately sized molecular phylogenies , 2015, Evolution; international journal of organic evolution.

[36]  David J. Lohman,et al.  When caterpillars attack: Biogeography and life history evolution of the Miletinae (Lepidoptera: Lycaenidae) , 2015, Evolution; international journal of organic evolution.

[37]  N. Pierce,et al.  Phylogeny of the Aphnaeinae: myrmecophilous African butterflies with carnivorous and herbivorous life histories , 2015 .

[38]  A. von Haeseler,et al.  IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies , 2014, Molecular biology and evolution.

[39]  J. Robertson,et al.  Explosive Adaptive Radiation and Extreme Phenotypic Diversity within Ant-Nest Beetles , 2014, Current Biology.

[40]  W. Bond,et al.  Savanna fire and the origins of the 'underground forests' of Africa. , 2014, The New phytologist.

[41]  M. Schulz,et al.  Uplift of Africa as a potential cause for Neogene intensification of the Benguela upwelling system , 2014 .

[42]  Camille Li,et al.  Aridification of the Sahara desert caused by Tethys Sea shrinkage during the Late Miocene , 2014, Nature.

[43]  Lisa N. Barrow,et al.  Species tree estimation of North American chorus frogs (Hylidae: Pseudacris) with parallel tagged amplicon sequencing. , 2014, Molecular phylogenetics and evolution.

[44]  H. Morlon.  Phylogenetic approaches for studying diversification. , 2014, Ecology letters.

[45]  K. Katoh,et al.  MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability , 2013, Molecular biology and evolution.

[46]  A. Lemmon,et al.  Anchored hybrid enrichment for massively high-throughput phylogenomics. , 2012, Systematic biology.

[47]  A. Lemmon,et al.  The venom-gland transcriptome of the eastern diamondback rattlesnake (Crotalus adamanteus) , 2012, BMC Genomics.

[48]  Verena D. Schmittmann,et al.  Qgraph: Network visualizations of relationships in psychometric data , 2012 .

[49]  Shane S. Sturrock,et al.  Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data , 2012, Bioinform..

[50]  H. Balslev,et al.  Cenozoic imprints on the phylogenetic structure of palm species assemblages worldwide , 2012, Proceedings of the National Academy of Sciences.

[51]  Simon H. Martin,et al.  Butterfly genome reveals promiscuous exchange of mimicry adaptations among species , 2012, Nature.

[52]  K. Gaston,et al.  The Fynbos and Succulent Karoo Biomes Do Not Have Exceptional Local Ant Richness , 2012, PloS one.

[53]  Shuai Zhan,et al.  The Monarch Butterfly Genome Yields Insights into Long-Distance Migration , 2011, Cell.

[54]  C. Marshall,et al.  The Molecular Phylogenetic Signature of Clades in Decline , 2011, PloS one.

[55]  Hélène Morlon,et al.  Reconciling molecular phylogenies with the fossil record , 2011, Proceedings of the National Academy of Sciences.

[56]  C. Strömberg.  Evolution of Grasses and Grassland Ecosystems , 2011 .

[57]  Tanja Stadler,et al.  Mammalian phylogeny reveals recent diversification rate shifts , 2011, Proceedings of the National Academy of Sciences.

[58]  Kurt E. Johnson,et al.  Phylogeny and palaeoecology of Polyommatus blue butterflies show Beringia was a climate-regulated gateway to the New World , 2011, Proceedings of the Royal Society B: Biological Sciences.

[59]  J. Ragle,et al.  IUCN Red List of Threatened Species , 2010 .

[60]  P. deMenocal,et al.  Global and African Regional Climate during the Cenozoic , 2010 .

[61]  Matthias Meyer,et al.  Illumina sequencing library preparation for highly multiplexed target capture and sequencing. , 2010, Cold Spring Harbor protocols.

[62]  Stephen A. Smith,et al.  The Origins of C4 Grasslands: Integrating Evolutionary and Ecosystem Science , 2010, Science.

[63]  O. Gascuel,et al.  New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. , 2010, Systematic biology.

[64]  N. Wahlberg,et al.  Out-of-Africa again: a phylogenetic hypothesis of the genus Charaxes (Lepidoptera: Nymphalidae) based on five gene regions. , 2009, Molecular phylogenetics and evolution.

[65]  M. Kuhlmann.  Patterns of diversity, endemism and distribution of bees (Insecta: Hymenoptera: Anthophila) in southern Africa , 2009 .

[66]  W. L. Distant,et al.  XX. On the Relationship between certain West African Insects, especially Ants, Lycaenidae and Homo-ptera , 2009 .

[67]  V. Savolainen,et al.  Origin and diversification of the Greater Cape flora: ancient species repository, hot-bed of recent radiation, or both? , 2009, Molecular phylogenetics and evolution.

[68]  Richard H. Ree,et al.  Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. , 2008, Systematic biology.

[69]  Ziheng Yang.  PAML 4: phylogenetic analysis by maximum likelihood. , 2007, Molecular biology and evolution.

[70]  G. Ramstein,et al.  Tectonic Uplift and Eastern Africa Aridification , 2006, Science.

[71]  R. Cowling,et al.  Insect diversity in Cape fynbos and neighbouring South African vegetation , 2006 .

[72]  Daniel L Rabosky,et al.  LASER: A Maximum Likelihood Toolkit for Detecting Temporal Shifts in Diversification Rates From Molecular Phylogenies , 2006, Evolutionary bioinformatics online.

[73]  T. Larsen.  Butterflies of West Africa , 2005 .

[74]  B. Jacobs.  Palaeobotanical studies from tropical Africa: relevance to the evolution of forest, woodland and savannah biomes. , 2004, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[75]  E. Paradis.  Can extinction rates be estimated without fossils? , 2004, Journal of theoretical biology.

[76]  P. deMenocal.  African climate change and faunal evolution during the Pliocene-Pleistocene , 2004 .

[77]  H. Linder,et al.  The radiation of the Cape flora, southern Africa , 2003, Biological reviews of the Cambridge Philosophical Society.

[78]  J. Giliomee.  Insect diversity in the Cape Floristic Region , 2003 .

[79]  M. Samways,et al.  Life history of the threatened Karkloof blue butterfly, Orachrysops ariadne (Lepidoptera : Lycaenidae) , 2001 .

[80]  M. Sanderson,et al.  ABSOLUTE DIVERSIFICATION RATES IN ANGIOSPERM CLADES , 2001, Evolution; international journal of organic evolution.

[81]  M. Cane,et al.  Closing of the Indonesian seaway as a precursor to east African aridification around 3–4 million years ago , 2001, Nature.

[82]  L. Sloan,et al.  Trends, Rhythms, and Aberrations in Global Climate 65 Ma to Present , 2001, Science.

[83]  A. Rosell‐Melé,et al.  Upwelling intensification as part of the Pliocene-Pleistocene climate transition. , 2000, Science.

[84]  N. Pierce,et al.  Phylogeny and life history evolution of the genus Chrysoritis within the Aphnaeini (Lepidoptera: Lycaenidae), inferred from mitochondrial cytochrome oxidase I sequences. , 2000, Molecular Phylogenetics and Evolution.

[85]  K. Fiedler.  REVIEW: Lycaenid-ant interactions of the Maculinea type: tracing their historical roots in a comparative framework , 1998, Journal of Insect Conservation.

[86]  A. Sourakov,et al.  Notes on life histories of Oboronia liberiana and Oboronia ornata (Lepidoptera: Lycaenidae). , 1997 .

[87]  R M May,et al.  Extinction rates can be estimated from molecular phylogenies. , 1994, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[88]  J. Thomas,et al.  Specialized searching and the hostile use of allomones by a parasitoid whose host, the butterfly Maculinea rebeli, inhabits ant nests , 1993, Animal Behaviour.

[89]  M. Alfaro,et al.  How Well Can We Estimate Diversity Dynamics for Clades in Diversity Decline? , 2019, Systematic biology.

[90]  A. Lemmon,et al.  Resolving Relationships among the Megadiverse Butterflies and Moths with a Novel Pipeline for Anchored Phylogenomics , 2018, Systematic biology.

[91]  D. A. Edge,et al.  Larval feeding behaviour and myrimecophily of the Brenton blue, Orachrysops niobe (Trimen) (Lepidoptera: Lycaenidae) , 2010, The Journal of Research on the Lepidoptera.

[92]  David J. Lohman,et al.  The ecology and evolution of ant association in the Lycaenidae (Lepidoptera). , 2002, Annual review of entomology.

[93]  L. Jacobs,et al.  The Origin of Grass-Dominated Ecosystems , 1999 .

[94]  Gerald H. Haug,et al.  Effect of the formation of the Isthmus of Panama on Atlantic Ocean thermohaline circulation , 1998, Nature.

[95]  N. Pierce.  Predatory and parasitic Lepidoptera: carnivores living on plants. , 1995 .

[96]  K. Fiedler.  Systematic, evolutionary, and ecological implications of myrmecophily within the Lycaenidae (Insecta: Lepidoptera: Papilionoidea) , 1991 .

[97]  C. Cottrell.  Aphytophagy in butterflies: its relationship to myrmecophily , 1984 .

[98]  P. Raven,et al.  Late Cretaceous and Tertiary vegetation history of Africa , 1978 .

[99]  J. Eliot.  The higher classification of the Lycaenidae (Lepidoptera): a tentative arrangement , 1973 .