André V. L. Freitas

Nymphalid butterflies diversify following near demise at the cretaceous/tertiary boundary

The butterfly family Nymphalidae contains some of the most important non-drosophilid insect model systems for evolutionary and ecological studies, yet the evolutionary history of the group has remained shrouded in mystery. We have inferred a robust phylogenetic hypothesis based on sequences of 10 genes and 235 morphological characters for exemplars of 400 of the 540 valid nymphalid genera representing all major lineages of the family. By dating the branching events, we infer that Nymphalidae originated in the Cretaceous at 90 Ma, but that the ancestors of 10–12 lineages survived the end-Cretaceous catastrophe in the Neotropical and Oriental regions. Patterns of diversification suggest extinction of lineages at the Cretaceous/Tertiary boundary (65 Ma) and subsequent elevated speciation rates in the Tertiary.

Phylogeny of the Nymphalidae (Lepidoptera).

A generic-level phylogeny for the butterfly family Nymphalidae was produced by cladistic analysis of 234 characters from all life stages. The 95 species in the matrix (selected from the 213 studied) represent all important recognized lineages within this family. The analysis showed the taxa grouping into six main lineages. The basal branch is the Libytheinae, with the Danainae and Ithomiinae on the next branch. The remaining lineages are grouped into two main branches: the Heliconiinae-Nymphalinae, primarily flower-visitors (but including the fruit-attracted Coeini); and the Limenitidinae (sensu strictu), Biblidinae, and the satyroid lineage (Apaturinae, Charaxinae, Biinae, Calinaginae, Morphinae, Brassolinae, and Satyrinae), primarily fruit-attracted. Data partitions showed that the two data sets (immatures and adults) are very different, and a partitioned Bremer support analysis showed that the adult characters are the main source of conflict in the nodes of the combined analysis tree. This phylogeny includes the widest taxon coverage of any morphological study on Nymphalid butterflies to date, and supports the monophyly and relationships of most presently recognized subgroups, providing strong evidence for the presently accepted phylogenetic scheme.

Ants as Selective Agents on Herbivore Biology: Effects on the Behaviour of a Non-Myrmecophilous Butterfly

Larvae of the nymphalid butterfly Eunica bechina feed on young leaves of Caryocar brasiliense, a shrub of the Brazilian savannah that is frequently visited by nectar-gathering ants. Eggs are not removed by ants, but ant occupation on plants affects the oviposition behaviour of the butterflies. Adult females avoid laying eggs on highly visited plant locations and visual cues were demonstrated to mediate oviposition by the butterflies. Plant branches with artificial rubber ants were significantly less infested than control branches with rubber circles. This is the first demonstration that ant presence per se can be enough to produce an avoidance response by ovipositing females in a non-myrmecophilous butterfly. Larval mortality was strongly affected by the level of ant visitation to the host plants, and vulnerability to ant predation decreased with larval size. Stick-like frass chains constructed by the larvae at leaf margins were demonstrated to be a safe refuge against ant attacks on the host plant. Live termites placed on leaves were attacked by foraging ants in significantly greater numbers than those placed on the frass chains. It is concluded that the behavioural biology of both immature and adult Eunica bechina is finely linked with the utilization of a host plant where ant visitation patterns strongly affect larval survival.

Out of the Andes: patterns of diversification in clearwing butterflies

Global biodiversity peaks in the tropical forests of the Andes, a striking geological feature that has likely been instrumental in generating biodiversity by providing opportunities for both vicariant and ecological speciation. However, the role of these mountains in the diversification of insects, which dominate biodiversity, has been poorly explored using phylogenetic methods. Here we study the role of the Andes in the evolution of a diverse Neotropical insect group, the clearwing butterflies. We used dated species‐level phylogenies to investigate the time course of speciation and to infer ancestral elevation ranges for two diverse genera. We show that both genera likely originated at middle elevations in the Andes in the Middle Miocene, contrasting with most published results in vertebrates that point to a lowland origin. Although we detected a signature of vicariance caused by the uplift of the Andes at the Miocene–Pliocene boundary, most sister species were parapatric without any obvious vicariant barrier. Combined with an overall decelerating speciation rate, these results suggest an important role for ecological speciation and adaptive radiation, rather than simple vicariance.

Butterfly Communities of Urban Forest Fragments in Campinas, São Paulo, Brazil: Structure, Instability, Environmental Correlates, and Conservation

A comparative study of butterfly communities in 15 urban/suburban remnants of tropical semideciduous forest in Campinas (São Paulo state, SE Brazil; 24°S, 47°W), with areas from 1.0 to 252 ha and widely varying histories and environments, shows that the most significant factors, besides area and sampling time, distinguishing the sites and influencing their diversity (80–702 species) and composition are connectivity, permanent water, vegetation, flowers, and human impact (negative, including pollution). The diversified Nymphalidae butterflies (38–213 species) and especially two fermented-bait-attracted groups (Satyrinae, 2–30 species, and Biblidini, 9–44 species), are among the more useful indicators of the quality and diversity of the environments in these fragments. Effective conservation of butterfly communities in tropical cities may be achieved by maintenance of arboreal green corridors along streets and watercourses between moderately large (>10 ha) humid areas, not near to the most built-up or polluted city centre(s), and the inclusion within these areas of ponds or streams, diversified native forest, and open vegetation including abundant nectar-rich flowers.

Egg-laying butterflies distinguish predaceous ants by sight.

Information about predation risks is critical for herbivorous insects, and natural selection favors their ability to detect predators before oviposition and to select enemy‐free foliage when offspring mortality risk is high. Food plants are selected by ovipositing butterflies, and offspring survival frequently varies among plants because of variation in the presence of predators. Eunica bechina butterflies oviposit on Caryocar brasiliense, an ant‐defended plant. Experiments with dried Camponotus and Cephalotes ants pinned to leaves revealed that butterflies use ant size and form as visual cues to avoid ovipositing on plant parts occupied by ants more likely to kill larval offspring. Presence of sap‐sucking bugs did not affect butterfly oviposition. This is the first demonstration that visual recognition of predators can mediate egg‐laying decisions by an insect herbivore and that an insect will discriminate among different species of potential predators. This unusual behavioral capability permits specialization on a risky, ant‐defended food plant.

Higher‐level phylogeny of the Ithomiinae (Lepidoptera: Nymphalidae): classification, patterns of larval hostplant colonization and diversification

We present a higher‐level phylogenetic hypothesis for the diverse neotropical butterfly subfamily Ithomiinae, inferred from one of the largest non‐molecular Lepidoptera data sets to date, including 106 species (105 ingroup) and 353 characters (306 informative) from adult and immature stage morphology and ecology. Initial analyses resulted in 1716 most parsimonious trees, which were reduced to a single tree after successive approximations character weighting. The inferred phylogeny was broadly consistent with other past and current work. Although some deeper relationships are uncertain, tribal‐level clades were generally strongly supported, with two changes required to existing classification. The tribe Melinaeini is polyphyletic and Athesis + Patricia require a new tribe. Methona should be removed from Mechanitini into the restored tribe Methonini. Dircennini was paraphyletic in analyses of all data but monophyletic based on adult morphology alone, and its status remains to be confirmed. Hypothyris, Episcada, Godyris, Hypoleria and Greta are paraphyletic. A simulation analysis showed that relatively basal branches tended to have higher partitioned Bremer support for immature stage characters. Larval hostplant records were optimized on to a reduced, generic‐level phylogeny and indicate that ithomiines moved from Apocynaceae to Solanaceae twice, or that Tithoreini re‐colonized Apocynaceae after a basal shift to Solanaceae. Ithomiine clades have specialized on particular plant clades suggesting repeated colonization of novel hostplant niches consistent with adaptive radiation. The shift to Solanum, comprising 70% of neotropical Solanaceae, occurs at the base of a clade containing 89% of all ithomiines, and is interpreted as the major event in the evolution of ithomiine larval hostplant relationships.

Biogeographic history of the butterfly subtribe Euptychiina (Lepidoptera, Nymphalidae, Satyrinae).

Peña, C., Nylin, S., Freitas, A. V. L. & Wahlberg, N. (2010). Biogeographic history of the butterfly subtribe Euptychiina (Lepidoptera, Nymphalidae, Satyrinae).—Zoologica Scripta, 39, 243–258.

Interaction between Mutualisms: Ant‐Tended Butterflies Exploit Enemy‐Free Space Provided by Ant‐Treehopper Associations

Although mutualisms have been intensively investigated, demonstration of indirect effects between co‐occurring mutualistic systems is rare. For instance, the ecological consequences of co‐occurrence of ant‐tended insects on a plant have never been examined for survival effects on either trophobiont species. Here, we assess the selective pressures mediating co‐occurrence of a facultative ant‐tended butterfly (Parrhasius polibetes) with ant‐tended treehoppers (Guayaquila xiphias) on Schefflera vinosa shrubs. We evaluated host plant selection and caterpillar survival in P. polibetes in the presence and absence of ant‐treehopper associations. Paired trials revealed that butterflies preferably oviposit on branches hosting ant‐tended treehoppers when they had a choice between those and branches without this interaction. Presence of ant‐tended treehoppers on a branch reduced the abundance of P. polibetes’ natural enemies and improved caterpillar survival in both premyrmecophylic and ant‐tended phases. Thus ant‐tended treehoppers create an enemy‐free space on foliage that butterflies exploit to protect larval offspring. These findings connect two widely documented ant‐trophobiont mutualisms and highlight the importance of considering multiple interactions for a proper understanding of ant‐plant‐herbivore systems. Detection of other ant‐based mutualisms on oviposition to improve offspring survival may have represented an important evolutionary step in the process of host plant selection in facultative myrmecophilous butterflies.

Phylogenetic relationships among the Ithomiini (Lepidoptera: Nymphalidae) inferred from one mitochondrial and two nuclear gene regions

Abstract.  A phylogenetic hypothesis for the tribe Ithomiini (Lepidoptera: Nymphalidae: Danainae) is presented, based on sequences of the mitochondrial cytochrome oxidase subunits I and II (COI–COII) region and regions of the nuclear genes wingless and Elongation factor 1‐alpha. Branch support for each clade is assessed, and a partition congruence index is used to explore conflict among gene regions. The monophyly of the clade is strongly supported, as are many of the traditionally recognized subtribes and genera. The data imply paraphyly of some genera and tribes, but largely support recent classifications and phylogenetic hypotheses based on morphological characters.