Phylogeography of Heliconius cydno and its closest relatives: disentangling their origin and diversification

The origins of the extraordinary diversity within the Neotropics have long fascinated biologists and naturalists. Yet, the underlying factors that have given rise to this diversity remain controversial. To test the relative importance of Quaternary climatic change and Neogene tectonic and paleogeographic reorganizations in the generation of biodiversity, we examine intraspecific variation across the Heliconius cydno radiation and compare this variation to that within the closely related Heliconius melpomene and Heliconius timareta radiations. Our data, which consist of both mtDNA and genome‐scan data from nearly 2250 amplified fragment length polymorphism (AFLP) loci, reveal a complex history of differentiation and admixture at different geographic scales. Both mtDNA and AFLP phylogenies suggest that H. timareta and H. cydno are probably geographic extremes of the same radiation that probably diverged from H. melpomene prior to the Pliocene–Pleistocene boundary, consistent with hypotheses of diversification that rely on geological events in the Pliocene. The mtDNA suggests that this radiation originated in Central America or the northwestern region of South America, with a subsequent colonization of the eastern and western slopes of the Andes. Our genome‐scan data indicate significant admixture among sympatric H. cydno/H. timareta and H. melpomene populations across the extensive geographic ranges of the two radiations. Within H. cydno, both mtDNA and AFLP data indicate significant population structure at local scales, with strong genetic differences even among adjacent H. cydno colour pattern races. These genetic patterns highlight the importance of past geoclimatic events, intraspecific gene flow, and local population differentiation in the origin and establishment of new adaptive forms.     

PATTERNS AND PROCESSES OF DIVERSIFICATION: SPECIATION AND HISTORICAL CONGRUENCE IN SOME NEOTROPICAL BIRDS

This paper documents congruence in geographical patterns of speciation for four clades of birds having taxa endemic to the same areas within the Neotropics. Two genera, Pionopsitta parrots and Selenidera toucans, corroborate a well known biogeographic disjunction in which taxa endemic to southern Central America and the Chocó region of northwestern South America are the sister-group to a radiation within the Amazon basin. These two genera, along with two lineages within the toucan genus Pteroglossus, also document a pattern of historical interrelationships for four well known areas of endemism within Amazonia: Guyanan + (Belém-Pará + (Inambari + Napo)). These generalized historical patterns are interpreted to have arisen via fragmentation (vicariance) of a widespread ancestral biota. A review of the paleogeographic evidence suggests that these vicariance events could have originated as a result of several different mechanisms operating at various times during the Cenozoic. The inference that diversification of the Neotropical biota is primarily the result of the most recent of these possible vicariance events, namely isolation within Quaternary forest refugia, is unwarranted, given present data. These patterns of historical congruence are also interpreted as direct evidence against the hypothesis that diversification of the forest biota was a consequence of parapatric differentiation along recently established ecological gradients.     

Phylogeny,Species Richness,and Ecological Specialization in Cyperaceae Tribe Cariceae

Cyperaceae tribe Cariceae is characterized by both species richness and habitat diversity, making it an ideal system to study ecological specialization and niche differentiation. We present a phylogenetic hypothesis for the tribe based on nuclear and chloroplast DNA sequence comparisons (ETS-1f, ITS, trnL intron, trnL-trnF intergenic spacer) for 140 representative species from five continents, and use this hypothesis to suggest patterns of both niche conservatism and niche differentiation, particularly within the large subgenus Carex. We identify a new major clade, comprising forest species of East Asian Carex section Siderostictae (subgenus Carex) as sister to the rest of tribe Cariceae. Within Carex subgenus Carex, species tolerant of water-saturated habitats occur in only a few, apparently derived groups, with varying species richness. Clades of predominantly wetland species tend to have broad geographic distribution, often with sister species on different continents, suggesting recent dispersal. In contrast, species within several clades are predominantly forest specialists with distinct Asian and North American lineages. Niche segregation along environmental gradients, such as soil moisture or acidity, is quite common among closely related wetland species, but more difficult to demonstrate within upland forest groups. More complete sampling of species within both wetland and forest groups, combined with comparable sampling of environmental preferences and testing against null models, will be needed for more rigorous exploration of the observed patterns.     

The ecology and social behaviour of the Neotropical butterfly Heliconius xanthocles Bates in Colombia

The mimicry, population ecology¹, adult behaviour and life cycle of Heliconius xanthocles were studied at two sites in Colombian tropical forest. The results were compared with the known biology of other Heliconius species. H. xanthocles is probably unpalatable and is a Mullerian comimic of some other species. In the Amazon basin H. xanthocles belongs to the 'dennis ray' mimicry ring of the Heliconiini, which includes Eueides tales, H. bumeyi, H. elevatus, H. melpomene and H. erato. In the Rio Negro valley, where the latter species either do not exist or have different mimetic allegiances, the 'clennis-ray' pattern of H. xanthocles breaks down. The adults are pollen-feeders, like other Heliconius. but they also visit other food sources such as bird droppings. During a mark-recapture programme in the Rio Negro, adults were found to be almost entirely restricted to small areas near their foodplant Passiflorapraeacuta. Females were rarer than males, but this was probably due to a behavioural difference between the sexes. The males had a Fisher-Ford survival rate of 0.95 per day and a life expectancy of 19 days. Population size estimates of males were between 11 and 17 individuals. These estimates are lower than, but comparable to those for other Heliconius. Males as well as females visit the larval toodplant, and an adult male was observed hovering over a small group of larvae. The females lav batches of 12–41 eggs. The largest batch (41 eggs) was laid cooperatively by two females. The larvae are gregarious feeders on shoot-tips of Passiflora praeacuta. and all lile stages are described for the first time. Predation on the larvae by a bug is described. The pupa has a distinctive morphology unlike that of other Heliconius. The adult population ecology, mimicry and larval behaviour are discussed.     

Ancient forest fragmentation or recent radiation? Testing refugial speciation models in chameleons within an African biodiversity hotspot

Aim East Africa is one of the most biologically diverse regions, especially in terms of endemism and species richness. Hypotheses put forward to explain this high diversity invoke a role for forest refugia through: (1) accumulation of new species due to radiation within refugial habitats, or (2) retention of older palaeoendemic species in stable refugia. We tested these alternative hypotheses using data for a diverse genus of East African forest chameleons, Kinyongia. Location East Africa. Methods We constructed a dated phylogeny for Kinyongia using one nuclear and two mitochondrial markers. We identified areas of high phylogenetic diversity (PD) and evolutionary diversity (ED), and mapped ancestral areas to ascertain whether lineage diversification could best be explained by vicariance or dispersal. Results Vicariance best explains the present biogeographic patterns, with divergence between three major Kinyongia clades (Albertine Rift, southern Eastern Arc, northern Eastern Arc) in the early Miocene/Oligocene (> 20 Ma). Lineage diversification within these clades pre‐dates the Pliocene (> 6 Ma). These dates are much older than the Plio‐Pleistocene climatic shifts associated with cladogenesis in other East African taxa (e.g. birds), and instead point to a scenario whereby palaeoendemics are retained in refugia, rather than more recent radiations within refugia. Estimates of PD show that diversity was highest in the Uluguru, Nguru and East Usambara Mountains and several lineages (from Mount Kenya, South Pare and the Uluguru Mountains) stand out as being evolutionarily distinct as a result of isolation in forest refugia. PD was lower than expected by chance, suggesting that the phylogenetic signal is influenced by an unusually low number of extant lineages with long branch lengths, which is probably due to the retention of palaeoendemic lineages. Main conclusions The biogeographic patterns associated with Kinyongia are the result of long evolutionary histories in isolation. The phylogeny is dominated by ancient lineages whose origins date back to the early Miocene/Oligocene as a result of continental wide forest fragmentation and contraction due to long term climatic changes in Africa. The maintenance of palaeoendemic lineages in refugia has contributed substantially to the remarkably high biodiversity of East Africa.     

Comparative population genetics of a mimicry locus among hybridizing Heliconius butterfly species

The comimetic Heliconius butterfly species pair, H. erato and H. melpomene, appear to use a conserved Mendelian switch locus to generate their matching red wing patterns. Here we investigate whether H. cydno and H. pachinus, species closely related to H. melpomene, use this same switch locus to generate their highly divergent red and brown color pattern elements. Using an F2 intercross between H. cydno and H. pachinus, we first map the genomic positions of two novel red/brown wing pattern elements; the G locus, which controls the presence of red vs brown at the base of the ventral wings, and the Br locus, which controls the presence vs absence of a brown oval pattern on the ventral hind wing. The results reveal that the G locus is tightly linked to markers in the genomic interval that controls red wing pattern elements of H. erato and H. melpomene. Br is on the same linkage group but approximately 26 cM away. Next, we analyze fine-scale patterns of genetic differentiation and linkage disequilibrium throughout the G locus candidate interval in H. cydno, H. pachinus and H. melpomene, and find evidence for elevated differentiation between H. cydno and H. pachinus, but no localized signature of association. Overall, these results indicate that the G locus maps to the same interval as the locus controlling red patterning in H. melpomene and H. erato. This, in turn, suggests that the genes controlling red pattern elements may be homologous across Heliconius, supporting the hypothesis that Heliconius butterflies use a limited suite of conserved genetic switch loci to generate both convergent and divergent wing patterns.     

Examination of the Taxonomy and Diversification of <Emphasis Type="Italic">Leontopithecus</Emphasis> using the Mitochondrial Control Region

Leontopithecus comprises 4 taxa: black lion tamarins (L. chrysopygus), golden lion tamarins (L. rosalia), black-faced lion tamarins (L. caissara), and golden-headed lion tamarins (L. chrysomelas). Endemic to the Atlantic Forest of Brazil, they are endangered (Appendix I, CITES; IUCN Critically Endangered: Leontopithecus chrysopygus, L. caissara; IUCN Endangered: L. rosalia, L. chrysomelas). The 4 taxa are differentiated morphologically and geographically and occupy different habitat types. However, it is not clear if all of them are separate species, particularly Leontopithecus caissara, or how they are related to one another evolutionarily. Therefore, we investigated lion tamarin differentiation and radiation. We sequenced the mtDNA control region and performed phylogenetic analyses, population aggregation analyses, and Mantel tests for geographic/genetic correlation. Mitochondrial genetic data suggest 3 distinct lion tamarin clades (Leontopithecus chrysomelas; L. caissara; and L. chrysopygus/L. rosalia). Phylogenetic analysis also supports: 1) the basal lion tamarin is Leontopithecus chrysomelas, and not L. chrysopygus, 2) L. caissara is not subspecific to L. chrysopygus, and 3) Quaternary forest refugia may have shaped lion tamarin diversification via a pattern that does not follow the theory of metachromism. Even though mitochondrial genetic analyses do not unequivocally support the 4 lion tamarins as separate species, one should consider the 4 lion tamarins, with equal conservation priority based on the combination of morphological, genetic, and habitat differentiation. Each of them is an extremely valuable flagship species that focuses attention on the diminishing, highly endemic Atlantic Forest of Brazil.     

Implications of 19th century landscape patterns for the recovery of Fagus crenata forests

Questions: What is the effect of the 19th century (pre‐industrialization) landscape pattern on the recovery of climax forests in cool‐temperate mountain areas dominated by Fagus crenata (Japanese beech)? Location: Secondary forests on Mt. Daisen, western Japan. Methods: Vegetation patterns before and after industrialization were obtained from maps drawn in 1898 and 1979. Tree measurements were made in 12 plots in 1997. Correlation between current Fagus crenata dominance and forest edge in the 19th century was analysed using an S‐shaped regression curve. Fagus juvenile density was counted in the plots, and distances from each plot to the five nearest mother trees were measured to determine the dispersal kernel. Results: Secondary grassland covered a substantial area in 1898, whereas forest covered most of the area in 1997. Fagus was dominant in places in the interior forest 100 years ago, and mature Fagus trees were absent in secondary forests that had been grasslands in 1898. The expected number of juveniles decreased to one individual per 100 m² at 43.5 m from the mother tree. Conclusions: The pre‐industrialization landscape greatly affected recovery of Fagus forest. Forests found on the 1898 vegetation map might have acted as refugia for Fagus. The limited dispersal ability of Fagus suggests that it would take many generations (several hundred years) for Fagus forests to recover at the centre of what had been grasslands in the 19th century.     

Identification of glacial refugia in south-eastern North America by phylogeographical analyses of a forest understorey plant, Trillium cuneatum

Aim We examine several hypotheses emerging from biogeographical and fossil records regarding glacial refugia of a southern thermophilic plant species. Specifically, we investigated the glacial history and post‐glacial colonization of a forest understorey species, Trillium cuneatum. We focused on the following questions: (1) Did T. cuneatum survive the Last Glacial Maximum (LGM) in multiple refugia, and (if so) where were they located, and is the modern genetic structure congruent with the fossil record‐based reconstruction of refugia for mesic deciduous forests? (2) What are the post‐glacial colonization patterns in the present geographical range? Location South‐eastern North America. Methods We sampled 45 populations of T. cuneatum throughout its current range. We conducted phylogeographical analyses based on maternally inherited chloroplast DNA (cpDNA haplotypes) and used TCS software to reconstruct intraspecific phylogeny. Results We detected six cpDNA haplotypes, geographically highly structured into non‐overlapping areas. With one exception, none of the populations had mixed haplotype composition. TCS analysis resulted in two intraspecific cpDNA lineages, with one clade subdivided further by shallower diversification. Main conclusions Our investigation revealed that T. cuneatum survived the LGM in multiple refugia, belonging to two (western, eastern) genealogical lineages geographically structured across south‐eastern North America. The western clade is confined to the south‐western corner of T. cuneatum’s modern range along the Lower Mississippi Valley, where fossil records document a major refugium of mesic deciduous forest. For the eastern clade, modern patterns of cpDNA haplotype distribution suggest cryptic vicariance, in the form of forest contractions and subsequent expansions associated with Pleistocene glacial cycles, rather than simple southern survival and subsequent northward colonization. The north–south partitioning of cpDNA haplotypes was unexpected, suggesting that populations of this rather southern thermophilic species may have survived in more northern locations than initially expected based on LGM climate reconstruction, and that the Appalachian Mountains functioned as a barrier to the dispersal of propagules originating in more southern refugia. Furthermore, our results reveal south‐west to north‐east directionality in historical migration through the Valley and Ridge region of north‐west Georgia.     

The roles of rivers and Pleistocene refugia in shaping genetic diversity in Praomys misonnei in tropical Africa

Aim This study aims to elucidate the phylogeography of the murid rodent Praomys misonnei and to document whether or not rain forest refugia and rivers structure patterns of diversity within this species. Location Tropical Africa, from Ghana to Kenya. Methods Patterns of genetic structure and signatures of population history (cytochrome b gene) were assessed in a survey of 229 individuals from 54 localities. Using maximum likelihood, Bayesian, network and genetic structure analyses, we inferred intra‐specific relationships and tested hypotheses for historical patterns of gene flow within P. misonnei. Results Our phylogenetic analyses reveal a strong phylogeographical structure. We identified four major geographical clades within P. misonnei: one clade in Ghana and Benin, a Nigerian clade, a West Central African clade and a Central and East African clade. Several subclades were identified within these four major clades. A signal of population expansion was detected in most clades or subclades. Coalescence within all of the major clades of P. misonnei occurred during the Middle Pleistocene and/or the beginning of Late Pleistocene. Main conclusions Our results suggest a role for both Pleistocene refugia and rivers in structuring genetic diversity in P. misonnei. This forest‐dwelling rodent may have been isolated in a number of forest fragments during arid periods and expanded its range during wetter periods. Potential forest refugia may have been localized in Benin–Ghana, south‐western Cameroon, southern Gabon, northern Gabon and eastern Democratic Republic of Congo–western Uganda. The Niger and/or the Cross Rivers, the Oubangui‐Congo, Sanaga, Ogooue and/or Ivindo Rivers probably stopped the re‐expansion of the species from relict areas.     

Resilient forest faunal communities in South Africa: a legacy of palaeoclimatic change and extinction filtering?

Aim To examine the influence of climatic extinction filtering during the last glacial maximum (LGM; c. 18,000 yr bp ) and of the subsequent recolonization of forest faunas on contemporary assemblage composition in southern African forests. Location South Africa, Mozambique, Swaziland, Zimbabwe. Methods Data comprised presence/absence by quarter‐degree grid cell for forest‐dependent and forest‐associated birds, non‐volant mammals and frogs. Twenty‐one forest subregions were assigned to one of three previously identified forest types: Afrotemperate, scarp, and Indian Ocean coastal belt. Differences among forest types were examined through patterns and gradients of species richness and endemism, assemblage similarity, species turnover, and coefficients of species dispersal direction. The influence of contemporary environment on assemblage composition was investigated using partial canonical correspondence analysis. Several alternative biogeographical hypotheses for the recolonization of forest faunas were tested. Results Afrotemperate faunas are relatively species‐poor, have low species turnover, and are unsaturated and infiltrated by generalist species. In northern and central regions, communities are supplemented by recolonization from scarp forest refugia, and among frogs by autochthanous speciation in localized refugia. Scarp faunas are relatively species‐rich, contain many forest‐dependent species, have high species turnover, and overlap with coastal and Afrotemperate faunas. Coastal forests are relatively species‐rich with high species turnover. Main conclusions Afrotemperate communities were affected most by climatic extinction filtering events. Scarp forests were Afrotemperate refugia during the LGM and are a contemporary overlap zone between Afrotemperate and coastal forest. Coastal faunas derive from post‐LGM colonization along the eastern seaboard from tropical East African refugia. The greatest diversity is achieved in scarp and coastal forest faunas in northern KwaZulu–Natal province. This historical centre of diversity has influenced the faunal diversity of nearly all other forests in South Africa. The response of vertebrate taxa to large‐scale, historical processes is dependent on their relative mobility: forest birds best illustrate patterns resulting from post‐glacial faunal dispersal, while among mammals and frogs the legacy of climatic extinction filtering remains stronger.     

Post-glacial range formation of temperate forest understorey herbs – Insights from a spatio-temporally explicit modelling approach

Aim

Our knowledge of Pleistocene refugia and post-glacial recolonization routes of forest understorey plants is still very limited. The geographical ranges of these species are often rather narrow and show highly idiosyncratic, often fragmented patterns indicating either narrow and species-specific ecological tolerances or strong dispersal limitations. However, the relative roles of these factors are inherently difficult to disentangle.

Location

Central and south-eastern Europe.

Time period

17,100 BP – present.

Major taxa studied

Five understorey herbs of European beech forests: Aposeris foetida, Cardamine trifolia, Euphorbia carniolica, Hacquetia epipactis and Helleborus niger.

Methods

We used spatio-temporally explicit modelling to reconstruct the post-glacial range dynamics of the five forest understorey herbs. We varied niche requirements, demographic rates and dispersal abilities across plausible ranges and simulated the spread of species from potential Pleistocene refugia identified by phylogeographical analyses. Then we identified the parameter settings allowing for the most accurate reconstruction of their current geographical ranges.

Results

We found a largely homogenous pattern of optimal parameter settings among species. Broad ecological niches had to be combined with very low but non-zero rates of long-distance dispersal via chance events and low rates of seed dispersal over moderate distances by standard dispersal vectors. However, long-distance dispersal events, although rare, led to high variation among replicated simulation runs.

Main conclusions

Small and fragmented ranges of many forest understorey species are best explained by a combination of broad ecological niches and rare medium- and long-distance dispersal events. Stochasticity is thus an important determinant of current species ranges, explaining the idiosyncratic distribution patterns of the study species despite strong similarities in refugia, ecological tolerances and dispersal abilities.     

First-generation linkage map of the warningly colored butterfly Heliconius erato

We report the first genetic linkage map of Heliconius erato, a species that shows remarkable variation in its warningly colored wing patterns. We use crosses between H. erato and its sister species, H. himera, to place two major color pattern genes, D and Cr, on a linkage map containing AFLP, allozyme, microsatellite and single-copy nuclear loci. We identified all 21 linkage groups in an initial genetic screen of 22 progeny from an F1 female x male H. himera family. Of the 229 markers, 87 used to identify linkage groups were also informative in 35 progeny from a sibling backcross (H. himera female x F1 male). With these, and an additional 33 markers informative in the second family, we constructed recombinational maps for 19 of the 21 linkage groups. These maps varied in length from 18.1 to 431.1 centimorgans (cM) and yielded an estimated total length of 2400 cM. The average distance between markers was 23 cM, and eight of the 19 linkage groups, including the sex chromosome (Z) and the chromosome containing the Cr locus, contained two or more codominant anchor loci. Of the three potential candidate genes mapped here, Cubitus interruptus (Ci), Decapentaplegic (Dpp) and Wingless (Wg), only Ci was linked, although loosely, to a known Heliconius color pattern locus. This work is an important first step for constructing a denser genetic map of the H. erato color pattern radiation and for a comparative genomic study of the architecture of mimicry in Heliconius butterflies.     

What can hybrid zones tell us about speciation? The case of Heliconius erato and H. himera (Lepidoptera: Nymphalidae)

To understand speciation we need to study the genetics and ecology of intermediate cases where interspecific hybridization still occurs. Two closely related species of Heliconius butterflies meet this criterion: Heliconius himera is endemic to dry forest and thorn scrub in southern Ecuador and northern Peru, while its sister species, H. erato , is ubiquitous in wet forest throughout south and central America. In three known zones of contact, the two species remain distinct, while hybrids are found at low frequency. Collections in southern Ecuador show that the contact zone is about 5 km wide, half the width of the narrowest clines between colour pattern races of H. erato. The narrowness of this dine argues that very strong selection (s ≅ 1) is maintaining the parapatric distributions of these two species. The zone is closely related with a habitat transition from wet to dry forest, which suggests that the narrow zone of parapatry is maintained primarily by ecological adaptation. Selection on colour pattern loci, assortative mating and hybrid inviability may also be important. The genetics of hybrids between the two species shows that the major gene control of pattern elements is similar to that found in previous studies of H. erato races, and some of the loci are homologous. This suggests that similar genetic processes are involved in the morphological divergence of species and races. Evidence from related Heliconius supports a hypothesis that ecological adaptation is the driving force for speciation in the group.     

In situ survival of forest bryophytes in small‐scale refugia after an intense forest fire

Question: Species can persist in landscapes with recurring disturbances either by migrating to places suitable for the moment or by enduring the threatening conditions. We investigated to what extent boreal forest bryophytes survived an intense forest fire in situ and whether bryophytes had started to recolonize the area 7‐8 years later. Location: Tyresta National Park, eastern Sweden. Methods: We recorded bryophytes in 14 burnt and 12 forest reference plots (50 × 50 m). In each plot we investigated 15 random 1‐m² micro‐plots. In plots in the burnt area we also examined micro‐plots at locations of all fire refugia, and in case of the forest references, of 10 potential refugia. Results: We found on average three small refugia per 50 × 50‐m plot; each containing on average 4.8 forest bryophytes, a level similar to that of micro‐plots in the references, but significantly higher than in random micro‐plots in the burnt plots (1.5 species). Many refugia were located in rocky areas, but few were in wet sites. The burnt area remained dominated by a few fire‐favoured species, even if recolonization of forest bryophytes had begun. There was, however, no significant correlation between number of refugia and number of forest species in random micro‐plots, leaving open the question of the importance of refugia as regulators of early succession. Conclusion: We conclude that small‐scale refugia can also occur for sensitive species such as forest bryophytes, and that the refugia in our case were frequently found on rocky or mesic rather than wet sites. The role of such refugia in recolonization, however, warrants further investigation.     

A hybrid zone provides evidence for incipient ecological speciation in Heliconius butterflies

In Heliconius butterflies, it has been proposed that speciation occurs through a combination of divergence in ecological habitat preferences and mimetic colour patterns. Here we test this hypothesis by investigating a parapatric form of the widespread species Heliconius erato. Mendelian (colour patterns) and molecular genetic data permit us to address hypotheses about introgression and genetic differentiation between different populations. Combined analysis of colour pattern, microsatellite loci and mitochondrial DNA showed that Heliconius erato venus and Heliconius erato chestertonii form a bimodal hybrid zone implying partial reproductive isolation. In a sample of 121 individuals collected in sympatry, 25% were hybrids representing a significant deficit of heterozygotes compared to the Hardy-Weinberg expectation. Seven microsatellite loci, analysed for a subset of these individuals, showed marked differentiation between the parental taxa, and unambiguously identified two genotypic clusters concordant with our phenotypic classification of individuals. Mitochondrial DNA analysis showed H. erato venus as a monophyletic group well differentiated from H. erato chestertonii, implying a lack of historical introgression between the populations. Heliconius erato chestertonii is therefore an incipient species that maintains its integrity despite high levels of hybridization. Moreover, H. erato chestertonii is found at higher altitudes than other races of H. erato and has a distinct colour pattern and mimetic relationship. Hence, there are now two examples of parapatric incipient species related to H. erato, H. himera and H. erato chestertonii, both of which are associated with higher altitudes, more arid habitats and distinct mimetic relationships. This implies that parapatric habitat adaptation is a likely cause of speciation in this group.     

Development of microsatellite loci from a reference genome for the Neotropical butterfly Heliconius numata and its close relatives

The Neotropical butterfly Heliconius numata (Lepidoptera: Nymphalidae: Heliconiinae) is known for its striking diversity of wing color patterns driven by the Müllerian mimicry of multiple local models and controlled by a single supergene locus. Such fine‐scale variation of traits under strong selection offers a unique opportunity for the study of the ecology and genetics of adaptation. However, little is still known of the population processes driving geographical variation in wing‐pattern phenotypes. We report the characterization of 26 microsatellite markers for the butterfly H. numata, including six located inside the wing color‐pattern supergene region. All markers are polymorphic, with allele numbers ranging from 2 to 21 per locus, an observed heterozygosity of 0.111 to 0.848 and an expected heterozygosity of 0.126 to 0.942. A subset of 18 of these markers was tested on five closely related sympatric Heliconius species with an amplification success ranging from 88% to 94%. The obtained set of microsatellite markers provides a new and useful set of tools to investigate patterns of differentiation and selection in populations of mimetic Heliconius butterflies. Moreover, markers developed within the color‐pattern supergene will facilitate characterization of the association between the genetic architecture and the functional diversity of wing patterns. Finally, the cross‐species amplification success of the described markers extends their utility to also encompass comparative population genetic studies of closely related species within a clade of rapidly diversifying species.     

Of glaciers and refugia: a decade of study sheds new light on the phylogeography of northwestern North America

Glacial cycles have played a dominant role in shaping the genetic structure and distribution of biota in northwestern North America. The two major ice age refugia of Beringia and the Pacific Northwest were connected by major mountain chains and bordered by the Pacific Ocean. As a result, numerous refugial options were available for the regions taxa during glacial advances. We reviewed the importance of glaciations and refugia in shaping northwestern North America’s phylogeographic history. We also tested whether ecological variables were associated with refugial history. The recurrent phylogeographic patterns that emerged were the following: (i) additional complexity, i.e. refugia within refugia, in both Beringia and the Pacific Northwest; and (ii) strong evidence for cryptic refugia in the Alexander Archipelago and Haida Gwaii, the Canadian Arctic and within the ice‐sheets. Species with contemporary ranges that covered multiple refugia, or those with high dispersal ability, were significantly more likely to have resided in multiple refugia. Most of the shared phylogeographic patterns can be attributed to multiple refugial locales during the last glacial maximum or major physiographic barriers like rivers and glaciers. However, some of the observed patterns are much older and appear connected to the orogeny of the Cascade‐Sierra chain or allopatric differentiation during historic glacial advances. The emergent patterns from this review suggest we should refine the classic Beringian‐southern refugial paradigm for northwestern North American biota and highlight the ecological and evolutionary consequences of colonization from multiple refugia.     

Seasonality and growth rings in lianas of Bignoniaceae

Lianas are one of the most important components of tropical forest, and yet one of the most poorly known organisms. Therefore, our paper addresses questions on the environmental and developmental aspects that influence the growth of lianas of Bignoniaceae, tribe Bignonieae. In order to better understand their growth, we studied the stem anatomy, seasonality of formation and differentiation of secondary tissues, and the influence of the cambial variant in xylem development on a selected species: Tynanthus cognatus. Afterwards, we compared the results found in T. cognatus with 31 other species of Bignonieae to identify general patterns of growth in lianas of this tribe. We found that cambial activity starts toward the end of the rainy season and onset of the dry season, in contrast to what is known for tropical trees and shrubs. Moreover, their pattern of xylem formation and differentiation is strongly influenced by the presence of massive wedges of phloem produced by a variant cambium. Thus, the variant cambium is the first to commence its activity and only subsequently does cambial activity progress towards the center of the regular region, leading to the formation of confluent growth rings. In summary, we conclude that: the cambium responds to environmental changes; the xylem growth rings are annual and produced in a brief period of about 2 months, something that may explain why lianas possess narrow stems; and furthermore, phloem wedges greatly influence cambial activity.