Recent diversification of Chrysoritis butterflies in the South African Cape (Lepidoptera: Lycaenidae)

Although best known for its extraordinary radiations of endemic plant species, the South African fynbos is home to a great diversity of phytophagous insects, including butterflies in the genus Chrysoritis (Lepidoptera: Lycaenidae). These butterflies are remarkably uniform morphologically; nevertheless, they comprise 43 currently accepted species and 68 currently valid taxonomic names. While many species have highly restricted, dot-like distributions, others are widespread. Here, we investigate the phylogenetic and biogeographic history underlying their diversification by analyzing molecular markers from 406 representatives of all described species throughout their respective ranges. We recover monophyletic clades for both C. chrysaor and C. thysbe species-groups, and identify a set of lineages that fall between them. The estimated age of divergence for the genus is 32 Mya, and we document significantly rapid diversification of the thysbe species-group in the Pleistocene (~2 Mya). Using ancestral geographic range reconstruction, we show that West Fynbos is the most likely region of origin for the radiation of the thysbe species-group. The colonization of this region occurred 9 Mya and appears to have been followed by a long period of relative stasis before a recent increase in diversification. Thus, the thysbe radiation does not appear to have resulted from the colonization of new biogeographic areas. Rather, the impact of species interactions (with ants and plants), the appearance of key innovations, and/or the opening of new ecological niche space in the region might explain the sudden burst of speciation that occurred in this group 2 Mya. The biogeographic model suggests two different diversification processes with few historical cross-colonisations, one in eastern South Africa for the C. chrysaor group and the other in western South Africa for the remaining taxa. Distributional range assessments and ecological niche models for each species show important niche overlap, and in a few cases, complete overlap. However, these shared traits are not explained by phylogenetic history. Chrysoritis taxa frequently fly in sympatry and gene tree reticulation appears to be widespread at the species level, suggesting that several episodes of range shifts might have led to secondary sympatries, allowing limited gene flow that challenges species delimitation efforts. In addition, the unusually high diversification rate for the thysbe clade of 1.35 [0.91–1.81] lineages per million years also suggests the possibility of taxonomic oversplitting. The phylogeny presented here provides a framework for a taxonomic revision of the genus. We highlight cases of potential synonymy both in allopatry and sympatry, and stress the importance of dedicated studies to assess potential pre- and post-zygotic barriers giving rise to species delimitations of the thysbe group.GT was supported by the MINECO programme Juan de la Cierva Incorporación (IJCI‐2016‐29083), the Marie Curie Actions FP7‐People‐2013 IOF (project 622716), “La Caixa” Foundation (LCF/BQ/PR19/11700004), and the National Geographic Society (grant #WW1‐300R‐18). ZAK was supported by an NSF Graduate Research Fellowship. Collecting expeditions were made possible by grants from the Putnam Expeditionary Fund of the Museum of Comparative Zoology (MCZ, Harvard University) to ZAK, and the research was supported by NSF DEB-0447244 and DEB-1541560 to NEP.Peer reviewe

When caterpillars attack: Biogeography and life history evolution of the Miletinae (Lepidoptera: Lycaenidae)

© 2015 The Author(s). Of the four most diverse insect orders, Lepidoptera contains remarkably few predatory and parasitic species. Although species with these habits have evolved multiple times in moths and butterflies, they have rarely been associated with diversification. The wholly aphytophagous subfamily Miletinae (Lycaenidae) is an exception, consisting of nearly 190 species distributed primarily throughout the Old World tropics and subtropics. Most miletines eat Hemiptera, although some consume ant brood or are fed by ant trophallaxis. A well-resolved phylogeny inferred using 4915 bp from seven markers sampled from representatives of all genera and nearly one-third the described species was used to examine the biogeography and evolution of biotic associations in this group. Biogeographic analyses indicate that Miletinae likely diverged from an African ancestor near the start of the Eocene, and four lineages dispersed between Africa and Asia. Phylogenetic constraint in prey selection is apparent at two levels: related miletine species are more likely to feed on related Hemiptera, and related miletines are more likely to associate with related ants, either directly by eating the ants, or indirectly by eating hemipteran prey that are attended by those ants. These results suggest that adaptations for host ant location by ovipositing female miletines may have been retained from phytophagous ancestors that associated with ants mutualistically.ZAK was funded by a National Science Foundation (NSF) Graduate Research Fellowship and DJL was funded by an Environmental Protection Agency Science to Achieve Results Fellowship and NSF DEB-1120380. Collecting expeditions were made possible by grants from the Putnam Expeditionary Fund of the Museum of Comparative Zoology to NEP and DJL, and the research was funded by NSF DEB-9615760 and NSF DEB-0447244 to NEP.Peer Reviewe

Gene Genealogies Strongly Distorted by Weakly Interfering Mutations in Constant Environments

Neutral nucleotide diversity does not scale with population size as expected, and this “paradox of variation” is especially severe for animal mitochondria. Adaptive selective sweeps are often proposed as a major cause, but a plausible alternative is selection against large numbers of weakly deleterious mutations subject to Hill–Robertson interference. The mitochondrial genealogies of several species of whale lice (Amphipoda: Cyamus) are consistently too short relative to neutral-theory expectations, and they are also distorted in shape (branch-length proportions) and topology (relative sister-clade sizes). This pattern is not easily explained by adaptive sweeps or demographic history, but it can be reproduced in models of interference among forward and back mutations at large numbers of sites on a nonrecombining chromosome. A coalescent simulation algorithm was used to study this model over a wide range of parameter values. The genealogical distortions are all maximized when the selection coefficients are of critical intermediate sizes, such that Muller's ratchet begins to turn. In this regime, linked neutral nucleotide diversity becomes nearly insensitive to N. Mutations of this size dominate the dynamics even if there are also large numbers of more strongly and more weakly selected sites in the genome. A genealogical perspective on Hill–Robertson interference leads directly to a generalized background-selection model in which the effective population size is progressively reduced going back in time from the present

Population histories of right whales (Cetacea: \u3ci\u3eEubalaena\u3c/i\u3e) Inferred from Mitochondrial Sequence Diversities and Divergences of Their Whale Lice (Amphipoda: \u3ci\u3eCyamus\u3c/i\u3e)

Right whales carry large populations of three ‘whale lice’ (Cyamus ovalis, Cyamus gracilis, Cyamus erraticus) that have no other hosts. We used sequence variation in the mitochondrial COI gene to ask (i) whether cyamid population structures might reveal associations among right whale individuals and subpopulations, (ii) whether the divergences of the three nominally conspecific cyamid species on North Atlantic, North Pacific, and southern right whales (Eubalaena glacialis, Eubalaena japonica, Eubalaena australis) might indicate their times of separation, and (iii) whether the shapes of cyamid gene trees might contain information about changes in the population sizes of right whales. We found high levels of nucleotide diversity but almost no population structure within oceans, indicating large effective population sizes and high rates of transfer between whales and subpopulations. North Atlantic and Southern Ocean populations of all three species are reciprocally monophyletic, and North Pacific C. erraticus is well separated from North Atlantic and southern C. erraticus. Mitochondrial clock calibrations suggest that these divergences occurred around 6 million years ago (Ma), and that the Eubalaena mitochondrial clock is very slow. North Pacific C. ovalis forms a clade inside the southern C. ovalis gene tree, implying that at least one right whale has crossed the equator in the Pacific Ocean within the last 1–2 million years (Myr). Low-frequency polymorphisms are more common than expected under neutrality for populations of constant size, but there is no obvious signal of rapid, interspecifically congruent expansion of the kind that would be expected if North Atlantic or southern right whales had experienced a prolonged population bottleneck within the last 0.5 Myr

Dataset from: Rapid radiation of ant parasitic butterflies during the Miocene aridification of Africa

Description of the files: 2_PHASED_ALIGNMENTS: Individual phased alignments used as input to produce gene trees in IQ-TREE. In fasta format.-- 3_UNPHASED_ALIGNMENTS: Individual alignments used to produce the full ML tree. In fasta format.-- 4_CONCATENATED_ALIGNMENT: The full concatenated alignment in phylip format and a .nex file with the models and partition scheme.-- 5_DATING: Concatenated reduced alignment in phylip format and the fixed input tree in Newick format used for dating. Taxon names were renamed since MCMCtree cannot handle taxon names longer than 49 characters. The file Rename.txt can be used to rename files back to the original names using sed: sed -f Rename.txt file > renamed_file. Convergence_plots.pdf contains plots of the mean age and upper and lower 95% highest posterior density (HPD) credibility intervals of two and two MCMCtree runs against each other to assure convergence of MCMC chains.-- 6_GENETREES: Genetrees used for input in ASTRAL. In Newick format.-- 7_FINAL_TREES: The ASTRAL species tree (Fig. S2), full ML tree (Fig. S1) and reduced, dated ML tree (Fig. 1, Fig. S4), with only on specimen included per species. The dated tree is in nexus format, and the others in Newick format.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.Peer reviewe

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