Renewed diversification is associated with new ecological opportunity in the Neotropical turtle ants

Ecological opportunity, defined as access to new resources free from competitors, is thought to be a catalyst for the process of adaptive radiation. Much of what we know about ecological opportunity, and the larger process of adaptive radiation, is derived from vertebrate diversification on islands. Here, we examine lineage diversification in the turtle ants (Cephalotes), a species‐rich group of ants that has diversified throughout the Neotropics. We show that crown group turtle ants originated during the Eocene (around 46 mya), coincident with global warming and the origin of many other clades. We also show a marked lineage‐wide slowdown in diversification rates in the Miocene. Contrasting this overall pattern, a species group associated with the young and seasonally harsh Chacoan biogeographic region underwent a recent burst of diversification. Subsequent analyses also indicated that there is significant phylogenetic clustering within the Chacoan region and that speciation rates are highest there. Together, these findings suggest that recent ecological opportunity, from successful colonization of novel habitat, may have facilitated renewed turtle ant diversification. Our findings highlight a central role of ecological opportunity within a successful continental radiation.     

Rapid diversification of Tragopogon and ecological associates in Eurasia

Tragopogon comprises approximately 150 described species distributed throughout Eurasia from Ireland and the UK to India and China with a few species in North Africa. Most of the species diversity is found in Eastern Europe to Western Asia. Previous phylogenetic analyses identified several major clades, generally corresponding to recognized taxonomic sections, although relationships both among these clades and among species within clades remain largely unresolved. These patterns are consistent with rapid diversification following the origin of Tragopogon, and this study addresses the timing and rate of diversification in Tragopogon. Using BEAST to simultaneously estimate a phylogeny and divergence times, we estimate the age of a major split and subsequent rapid divergence within Tragopogon to be ~2.6 Ma (and 1.7–5.4 Ma using various clock estimates). Based on the age estimates obtained with BEAST (HPD 1.7–5.4 Ma) for the origin of crown group Tragopogon and 200 estimated species (to accommodate a large number of cryptic species), the diversification rate of Tragopogon is approximately 0.84–2.71 species/Myr for the crown group, assuming low levels of extinction. This estimate is comparable in rate to a rapid Eurasian radiation in Dianthus (0.66–3.89 species/Myr), which occurs in the same or similar habitats. Using available data, we show that subclades of various plant taxa that occur in the same semi‐arid habitats of Eurasia also represent rapid radiations occurring during roughly the same window of time (1.7–5.4 Ma), suggesting similar causal events. However, not all species‐rich plant genera from the same habitats diverged at the same time, or at the same tempo. Radiations of several other clades in this same habitat (e.g. Campanula, Knautia, Scabiosa) occurred at earlier dates (45–4.28 Ma). Existing phylogenetic data and diversification estimates therefore indicate that, although some elements of these semi‐arid communities radiated during the Plio‐Pleistocene period, other clades sharing the same habitat appear to have diversified earlier.     

Divergence in brain composition during the early stages of ecological specialization in Heliconius butterflies

During speciation across ecological gradients, diverging populations are exposed to contrasting sensory and spatial information that present new behavioural and perceptive challenges. These challenges may be met by heritable or environmentally induced changes in brain function which mediate behaviour. However, few studies have investigated patterns of neural divergence at the early stages of speciation, inhibiting our understanding of the relative importance of these processes. Here, we provide a novel case study. The incipient species pair, Heliconius erato and H. himera, are parapatric across an environmental and altitudinal gradient. Despite ongoing gene flow, these species have divergent ecological, behavioural and physiological traits. We demonstrate that these taxa also differ significantly in brain composition, in particular in the relative levels of investment in structures that process sensory information. These differences are not explained solely by environmentally‐induced plasticity, but include heritable, nonallometric shifts in brain structure. We suggest these differences reflect divergence to meet the demands of contrasting sensory ecologies. This conclusion would support the hypothesis that the evolution of brain structure and function play an important role in facilitating the emergence of ecologically distinct species.     

Rapid diversification and not clade age explains high diversity in neotropical Adelpha butterflies

Latitudinal gradients in species richness are among the most well-known biogeographic patterns in nature, and yet there remains much debate and little consensus over the ecological and evolutionary causes of these gradients. Here, we evaluated whether two prominent alternative hypotheses (namely differences in diversification rate or clade age) could account for the latitudinal diversity gradient in one of the most speciose neotropical butterfly genera (Adelpha) and its close relatives. We generated a multilocus phylogeny of a diverse group of butterflies in the containing tribe Limenitidini, which has both temperate and tropical representatives. Our results suggest there is no relationship between clade age and species richness that could account for the diversity gradient, but that instead it could be explained by a significantly higher diversification rate within the predominantly tropical genus Adelpha. An apparent early larval host-plant shift to Rubiaceae and other plant families suggests that the availability of new potential host plants probably contributed to an increase in diversification of Adelpha in the lowland Neotropics. Collectively, our results support the hypothesis that the equatorial peak in species richness observed within Adelpha is the result of increased diversification rate in the last 10-15 Myr rather than a function of clade age, perhaps reflecting adaptive divergence in response to the dramatic host-plant diversity found within neotropical ecosystems.     

Patterns of host plant utilization and diversification in the brush‐footed butterflies

Herbivorous insects represent one of the most successful animal radiations known. They occupy a wide range of niches, feed on a great variety of plants, and are species rich; yet the factors that influence their diversification are poorly understood. Host breadth is often cited as a major factor influencing diversification, and, according to the Oscillation Hypothesis, shifts from generalist to specialist feeding states increase the diversification rate for a clade. We explored the relationship between host breadth and diversification within the Nymphalidae (Lepidoptera) and explicitly tested predictions of the Oscillation Hypothesis. We found strong evidence of diversification rate heterogeneity, but no difference in host breadth between clades with a higher diversification rate compared to their sisters. We also found some clades exhibited phylogenetic nonindependence in host breadth and these clades had lower host plant turnover than expected by chance, suggesting host breadth is evolutionarily constrained. Finally, we found that transitions among host breadth categories varied, but the likelihood of reductions in host breadth was greater than that of increases. Our results indicate host breadth is decoupled from diversification rate within the Nymphalidae, and that constraints on diet breadth might play an important role in the evolution of herbivorous insects.     

Dynamics of host plant use and species diversity in Polygonia butterflies (Nymphalidae)

The ability of insects to utilize different host plants has been suggested to be a dynamic and transient phase. During or after this phase, species can shift to novel host plants or respecialize on ancestral ones. Expanding the range of host plants might also be a factor leading to higher levels of net speciation rates. In this paper, we have studied the possible importance of host plant range for diversification in the genus Polygonia (Nymphalidae, Nymphalini). We have compared species richness between sistergroups in order to find out if there are any differences in number of species between clades including species that utilize only the ancestral host plants ('urticalean rosids') and their sisterclades with a broader (or in some cases potentially broader) host plant repertoire. Four comparisons could be made, and although these are not all phylogenetically or statistically independent, all showed clades including butterfly species using other or additional host plants than the urticalean rosids to be more species-rich than their sisterclade restricted to the ancestral host plants. These results are consistent with the theory that expansions in host plant range are involved in the process of diversification in butterflies and other phytophagous insects, in line with the general theory that plasticity may drive speciation.     

Rapid evolution and specialization following host colonization in a yucca moth

Host shifts followed by specialization can result in sympatric genetic differentiation, and may have fuelled the diversification of phytophagous insects. This study examines a recent colonization of a non‐native host by Prodoxus quinquepunctellus (Lepidoptera: Prodoxidae). Allozyme differentiation was detected among different host feeding populations, yet was nearly absent among similar host feeding populations in sympatry. Geographical patterns of allozyme variation showed a much higher level of population structure among populations feeding on the derived host. Conversely, mtDNA haplotype frequencies were nearly homogeneous in the derived populations compared to the ancestral populations, suggesting a bottleneck and/or rapid fixation of haplotypes following host colonization. Moth emergence coincided with host plant flowering, and phenological differences between host species translated into allochronic isolation between populations feeding on different hosts. Derived moth populations also differed significantly in three ovipositor characters from ancestral populations. These findings suggest rapid host‐specific genetic differentiation, and specialization of moth emergence time and ovipositor morphology following host colonization.     

Divergent host plant specialization as the critical driving force in speciation between populations of a phytophagous ladybird beetle

Detecting the isolating barrier that arises earliest in speciation is critically important to understanding the mechanism of species formation. We tested isolating barriers between host races of a phytophagous ladybird beetle, Henosepilachna diekei (Coleoptera: Coccinellidae: Epilachnine), that occur sympatrically on distinct host plants. We conducted field surveys for the distribution of the beetles and host plants, rearing experiments to measure six potential isolating factors (adult host preference, adult and larval host performance, sexual isolation, egg hatchability, F(1) hybrid inviability, and sexual selection against F(1) hybrids), and molecular analyses of mitochondrial ND2 and the nuclear ITS2 sequences. We found significant genetic divergence between the host races, and extremely divergent host preference (i.e. habitat isolation) and host performance (i.e. immigrant inviability), but no other isolating barriers. The fidelity to particular host plants arises first and alone can prevent gene flow between differentiating populations of phytophagous specialists.     

Use it or lose it: reproductive implications of ecological specialization in a haematophagous ectoparasite

Using experimentally induced disruptive selection, we tested two hypotheses regarding the evolution of specialization in parasites. The 'trade-off' hypothesis suggests that adaptation to a specific host may come at the expense of a reduced performance when exploiting another host. The alternative 'relaxed selection' hypothesis suggests that the ability to exploit a given host would deteriorate when becoming obsolete. Three replicate populations of a flea Xenopsylla ramesis were maintained on each of two rodent hosts, Meriones crassus and Dipodillus dasyurus, for nine generations. Fleas maintained on a specific host species for a few generations substantially decreased their reproductive performance when transferred to an alternative host species, whereas they generally did not increase their performance on their maintenance host. The results support the 'relaxed selection' hypothesis of the evolution of ecological specialization in haematophagous ectoparasites, while suggesting that trade-offs are unlikely drivers of specialization. Further work is needed to study the extent by which the observed specializations are based on epigenetic or genetic modifications.     

Sympatric diversification vs. immigration: deciphering host‐plant specialization in a polyphagous insect,the stolbur phytoplasma vector Hyalesthes obsoletus (Cixiidae)

The epidemiology of vector transmitted plant diseases is highly influenced by dispersal and the host‐plant range of the vector. Widening the vector's host range may increase transmission potential, whereas specialization may induce specific disease cycles. The process leading to a vector's host shift and its epidemiological outcome is therefore embedded in the frameworks of sympatric evolution vs. immigration of preadapted populations. In this study, we analyse whether a host shift of the stolbur phytoplasma vector, Hyalesthes obsoletus from field bindweed to stinging nettle in its northern distribution range evolved sympatrically or by immigration. The exploitation of stinging nettle has led to outbreaks of the grapevine disease bois noir caused by a stinging nettle‐specific phytoplasma strain. Microsatellite data from populations from northern and ancestral ranges provide strong evidence for sympatric host‐race evolution in the northern range: Host‐plant associated populations were significantly differentiated among syntopic sites (0.054 < F_HT < 0.098) and constant over 5 years. While gene flow was asymmetric from the old into the predicted new host race, which had significantly reduced genetic diversity, the genetic identity between syntopic host‐race populations in the northern range was higher than between these populations and syntopic populations in ancestral ranges, where there was no evidence for genetic host races. Although immigration was detected in the northern field bindweed population, it cannot explain host‐race diversification but suggests the introduction of a stinging nettle‐specific phytoplasma strain by plant‐unspecific vectors. The evolution of host races in the northern range has led to specific vector‐based bois noir disease cycles.     

Contrasting patterns of Andean diversification among three diverse clades of Neotropical clearwing butterflies

The Neotropical region is the most biodiverse on Earth, in a large part due to the highly diverse tropical Andean biota. The Andes are a potentially important driver of diversification within the mountains and for neighboring regions. We compared the role of the Andes in diversification among three subtribes of Ithomiini butterflies endemic to the Neotropics, Dircennina, Oleriina, and Godyridina. The diversification patterns of Godyridina have been studied previously. Here, we generate the first time‐calibrated phylogeny for the largest ithomiine subtribe, Dircennina, and we reanalyze a published phylogeny of Oleriina to test different biogeographic scenarios involving the Andes within an identical framework. We found common diversification patterns across the three subtribes, as well as major differences. In Dircennina and Oleriina, our results reveal a congruent pattern of diversification related to the Andes with an Andean origin, which contrasts with the Amazonian origin and multiple Andean colonizations of Godyridina. In each of the three subtribes, a clade diversified in the Northern Andes at a faster rate. Diversification within Amazonia occurred in Oleriina and Godyridina, while virtually no speciation occurred in Dircennina in this region. Dircennina was therefore characterized by higher diversification rates within the Andes compared to non‐Andean regions, while in Oleriina and Godyridina, we found no difference between these regions. Our results and discussion highlight the importance of comparative approaches in biogeographic studies.     

Ecological specialization and morphological diversification in Greater Antillean boas

Colonization of islands can dramatically influence the evolutionary trajectories of organisms, with both deterministic and stochastic processes driving adaptation and diversification. Some island colonists evolve extremely large or small body sizes, presumably in response to unique ecological circumstances present on islands. One example of this phenomenon, the Greater Antillean boas, includes both small (<90 cm) and large (4 m) species occurring on the Greater Antilles and Bahamas, with some islands supporting pairs or trios of body‐size divergent species. These boas have been shown to comprise a monophyletic radiation arising from a Miocene dispersal event to the Greater Antilles, though it is not known whether co‐occurrence of small and large species is a result of dispersal or in situ evolution. Here, we provide the first comprehensive species phylogeny for this clade combined with morphometric and ecological data to show that small body size evolved repeatedly on separate islands in association with specialization in substrate use. Our results further suggest that microhabitat specialization is linked to increased rates of head shape diversification among specialists. Our findings show that ecological specialization following island colonization promotes morphological diversity through deterministic body size evolution and cranial morphological diversification that is contingent on island‐ and species‐specific factors.     

Host conservatism, host shifts and diversification across three trophic levels in two Neotropical forests

Host-parasite systems have been models for understanding the connection between shifts in resource use and diversification. Despite theoretical expectations, ambiguity remains regarding the frequency and importance of host switches as drivers of speciation in herbivorous insects and their parasitoids. We examine phylogenetic patterns with multiple genetic markers across three trophic levels using a diverse lineage of geometrid moths (Eois), specialist braconid parasitoids (Parapanteles) and plants in the genus Piper. Host-parasite associations are mapped onto phylogenies, and levels of cospeciation are assessed. We find nonrandom patterns of host use within both the moth and wasp phylogenies. The moth-plant associations in particular are characterized by small radiations of moths associated with unique host plants in the same geographic area (i.e. closely related moths using the same host plant species). We suggest a model of diversification that emphasizes an interplay of factors including host shifts, vicariance and adaptation to intraspecific variation within hosts.     

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.     

Phylogenetic evidence for the evolution of ecological specialization in Timema walking‐sticks

We used phylogenetic and ecological information to study the evolution of host‐plant specialization and colour polymorphism in the genus Timema, which comprises 14 species of walking‐sticks that are subject to strong selection for cryptic coloration on their host‐plants. Phylogenetic analysis indicated that this genus consists of three main lineages. Two of the lineages include highly generalized basal species and relatively specialized distal species, and one of the lineages comprises four specialized species. We tested for phylogenetic conservatism in the traits studied via randomizing host‐plant use, and the four basic Timema colour patterns, across the tips of the phylogeny, and determining if the observed number of inferred changes was significantly low compared to the distribution of numbers of inferred changes expected under the null model. This analysis showed that (1) host‐plant use has evolved nonrandomly, such that more closely related species tend to use similar sets of hosts and (2) colour pattern evolution exhibits considerable lability. Inference of ancestral states using maximum parsimony, under four models for the relative ease of gain and loss of plant hosts or colour morphs, showed that (1) for all models with gains of host‐plants even marginally more difficult than losses, and for most optimizations with gains and losses equally difficult, the ancestral Timema were generalized, feeding on the chaparral plants Ceanothus and Adenostoma and possibly other taxa, and (2) for all models with gains of colour morphs more difficult than losses, the ancestral Timema were polymorphic for colour pattern. Generation of null distributions of inferred ancestral states showed that the maximum‐parsimony inference of host‐plant generalization was most robust for the most speciose of the three main Timema lineages. Ancestral states were also inferred using maximum likelihood, after recoding host‐plant use and colour polymorphism as dichotomous characters. Likelihood analyses provided some support for inference of generalization in host‐plant use at ancestral nodes of the two lineages exhibiting mixtures of generalists and specialists, although levels of uncertainty were high. By contrast, likelihood analysis did not estimate ancestral colour morph patterns with any confidence, due to inferred rates of change that were high with respect to speciation rates. Information from biogeography, floristic history and the timing of diversification of the genus are compatible with patterns of inferred ancestral host‐plant use. Diversification in the genus Timema appears to engender three main processes: (1) increased specialization via loss of host‐plants, (2) retention of the same, single, host‐plant and (3) shifts to novel hosts to which lineages were ‘preadapted’ in colour pattern. Our evidence suggests that the radiation of this genus has involved multiple evolutionary transitions from individual‐level specialization (multiple‐niche polymorphism) to population‐level and species‐level specialization. Ecological studies of Timema suggest that such transitions are driven by diversifying selection for crypsis. This paper provides the first phylogeny‐based evidence for the macroevolutionary importance of predation by generalist natural enemies in the evolution of specialization.     

Evolutionary dynamics of host-plant specialization: a case study of the tribe Nymphalini

Two general patterns that have emerged from the intense studies on insect-host plant associations are a predominance of specialists over generalists and a taxonomic conservatism in host-plant use. In most insect-host plant systems, explanations for these patterns must be based on biases in the processes of host colonizations, host shifts, and specialization, rather than cospeciation. In the present paper, we investigate changes in host range in the nymphalid butterfly tribe Nymphalini, using parsimony optimizations of host-plant data on the butterfly phylogeny. In addition, we performed larval establishment tests to search for larval capacity to feed and survive on plants that have been lost from the female egg-laying repertoire. Optimizations suggested an ancestral association with Urticaceae, and most of the tested species showed a capacity to feed on Urtica dioica regardless of actual host-plant use. In addition, there was a bias among the successful establishments on nonhosts toward plants that are used as hosts by other species in the Nymphalini. An increased likelihood of colonizing ancestral or related plants could also provide an alternative explanation for the observed pattern that some plant families appear to have been colonized independently several times in the tribe. We also show that there is no directionality in host range evolution toward increased specialization, that is, specialization is not a dead end. Instead, changes in host range show a very dynamic pattern.     

Palatablility and escaping ability in Neotropical butterflies: tests with wild kingbirds (Tyrannus melancholicus, Tyrannidae)

The palatability and the ability of neotropical butterflies to escape after being detected, attacked and captured by wild kingbirds ( Tyrannus melancholicus Vieillot), was investigated by the release of 668 individuals of 98 butterfly species close to the birds, during their usual feeding activities. Most of the butterflies were attacked and eaten. Only the troidine swallowtails ( Parities and Battus ; Papilionidae) were consistently rejected on taste and elicited aversive behaviours in birds. Most other aposematic and/or mimetic species in the gehera Danaus and Lycorea (Danainae), Dione, Eueides and Heliconius (Heliconiinae), Hypothyris, Mechanitis and Melinaea (Ithomfinae), Biblis, Callicore and Diaethria (Limenitidinae) were generally eaten. Cryptic and non-mimetic species were always attacked and, if captured, they were also eaten. All Apaturinae, Charaxinae, Nymphalinae, Hesperidae, most Limenitidinae, Heliconiinag ( Agraulis, Dryas, Dryadula and Philaethria ) and Papilionidae ( Eurytides, Heraclides and Protesilaus ) were in this group. Results indicate that the learning process in kingbirds may demand a large mortality in prey populations, even among species generally accepted as unpalatable and aposematic. They also support the assertion that escaping ability and unpalatability evolved in butterflies as alternative strategies to avoid predation by birds. Mimetic relationships among several species are discussed. Evidence for the evolution of aposematism not related to unpalatability, but to escaping ability, was found for two hard-to-catch Morpho species.     

The roles of wing color pattern and geography in the evolution of Neotropical Preponini butterflies

Diversification rates and evolutionary trajectories are known to be influenced by phenotypic traits and the geographic history of the landscapes that organisms inhabit. One of the most conspicuous traits in butterflies is their wing color pattern, which has been shown to be important in speciation. The evolution of many taxa in the Neotropics has also been influenced by major geological events. Using a dated, species‐level molecular phylogenetic hypothesis for Preponini, a colorful Neotropical butterfly tribe, we evaluated whether diversification rates were constant or varied through time, and how they were influenced by color pattern evolution and biogeographical events. We found that Preponini originated approximately 28 million years ago and that diversification has increased through time consistent with major periods of Andean uplift. Even though some clades show evolutionarily rapid transitions in coloration, contrary to our expectations, these shifts were not correlated with shifts in diversification. Involvement in mimicry with other butterfly groups might explain the rapid changes in dorsal color patterns in this tribe, but such changes have not increased species diversification in this group. However, we found evidence for an influence of major Miocene and Pliocene geological events on the tribe''s evolution. Preponini apparently originated within South America, and range evolution has since been dynamic, congruent with Andean geologic activity, closure of the Panama Isthmus, and Miocene climate variability.