Papers

Wang et al. have recently outlined their thoughts on two ideas about species: the biological species concept (BSC), and the genic view of speciation. Although both are based on reproductive isolation, the genic view, they argue, is likely preferred due to the possibility of allowing considerable gene flow among species, which is arguably what recent genomic data shows. These data, however, mostly failed to distinguish between the BSC and the genic view according to Wang et al., because it could not be ruled out that the observed introgression occurred early in speciation, when both models allow gene flow. I propose that the lack of resolution in the authors' debate is chiefly due to the difficulty of deciding when speciation is "complete" under both views tested. I agree with Wang et al. that the study of reproductive isolation is worthwhile in order to understand speciation, but I prefer to use a simpler, third criterion for speciation: the acquisition of genetic differences that allow persistence of distinguishable populations in spite of geographic overlap and the potential for continued gene flow. Under this multilocus "genotypic cluster" view, gene flow may take place at any time after species are recognized, and we do not have to decide whether gene flow is early or late in the speciation process. I detail recent genomic evidence from Anopheles mosquitoes and Heliconius butterflies showing that such "leaky" species seem to be able to coexist in spite of massive levels of introgression, often among non-sister species that show hybrid sterility in one sex.

Following gene flow in butterfly genomes

The role of hybridization in evolution and species radiations has long been debated. In Heliconius butterflies, introgression was a major factor in their radiation, and the genetic variation it imparted into species is variable across the genome. Edelman et al. developed a new sequencing strategy and produced 20 Heliconius genomes (see the Perspective by Rieseberg). They also developed a means by which to identify genetic variation that originates from incomplete lineage sorting versus hybridization. Applying this model to their newly developed genomes, they investigated the evolutionary history of the genus and, in particular, the impact of introgression.

Science, this issue p. 594; see also p. 570.

We used 20 de novo genome assemblies to probe the speciation history and architecture of gene flow in rapidly radiating Heliconius butterflies. Our tests to distinguish incomplete lineage sorting from introgression indicate that gene flow has obscured several ancient phylogenetic relationships in this group over large swathes of the genome. Introgressed loci are underrepresented in low-recombination and gene-rich regions, consistent with the purging of foreign alleles more tightly linked to incompatibility loci. Here, we identify a hitherto unknown inversion that traps a color pattern switch locus. We infer that this inversion was transferred between lineages by introgression and is convergent with a similar rearrangement in another part of the genus. These multiple de novo genome sequences enable improved understanding of the importance of introgression and selective processes in adaptive radiation.

Aim
The landscape of the Neotropical region has undergone dynamic evolution throughout the Miocene, with the extensive Pebas wetland occupying western Amazonia between 23 and c. 10 Ma and the continuous uplift of the Andes mountains. The complex interaction between the Andes and Amazonia probably influenced the trajectory of Neotropical biodiversity, but evidence from time-calibrated phylogenies of groups that diversified during this period is lacking. We investigate the role of these landscape transformations in the dynamics of diversification in the Neotropical region using a 26-Myr-old endemic butterfly radiation. Location Neotropics. Time period Oligocene to present. Major taxa studied Ithomiini butterflies.

Methods
We generated one of the most comprehensive time-calibrated molecular phylogenies of a large clade of Neotropical insects, the butterfly tribe Ithomiini, comprising 340 species (87% of extant species) and spanning 26 Myr of diversification. We applied a large array of birth–death models and historical biogeography estimations to assess the dynamics of diversification and biotic interchanges, especially at the Amazonia–Andes interface.

Results
Our results suggest that the Amazonian Pebas wetland system played a major role in the timing and geography of diversification of Ithomiini, by constraining dispersal and diversification in the Amazon basin until c. 10 Ma. During the Pebas wetland period, Ithomiini diversification mostly took place in the Andes, where terrestrial habitats were not affected. An explosion of interchanges with Amazonia and with the Northern Andes accompanied the demise of the Pebas system (11–8 Ma) and was followed by local diversification in those areas, which led to a substantial renewal of diversification.

Main conclusions
Many studies on Neotropical diversity have focused only on the Andes, whereas we show that it is the waxing and waning of the Pebas mega-wetland, interacting with Andean uplift, that determined the timing and patterns of regional interchanges and diversification in Ithomiini.

The evolution of reproductive isolation via a switch in mimetic wing coloration has become the paradigm for speciation in aposematic Heliconius butterflies. Here, we provide a counterexample to this, by documenting two cryptic species within the taxon formerly considered Heliconius demeter Staudinger, 1897. Amplified fragment length polymorphisms identify two sympatric genotypic clusters in northern Peru, corresponding to subspecies Heliconius demeter ucayalensis H. Holzinger & R. Holzinger, 1975 and Heliconius demeter joroni ssp. nov. These subspecies are reciprocally monophyletic for the mitochondrial genes COI and COII and the nuclear gene Ef1α, and exhibit marked differences in larval morphology and host plant use. COI sequences from 13 of the 15 currently recognized subspecies show that mtDNA differences are reflected across the range of H. demeter, with a deep phylogenetic split between the southern and northern Amazonian races. As such, our data suggest vicariant speciation driven by disruptive selection for larval performance on different host plants. We raise Heliconius demeter eratosignis (Joicey & Talbot, 1925) to Heliconius eratosignis based on nomenclatural priority, a species also comprising H. eratosignis ucayalensis comb. nov. and three other southern Amazonian races. Heliconius demeter joroni spp. nov. remains within H. demeter s.s., along with northern Amazonian and Guianan subspecies.

Understanding why species richness peaks along the Andes is a fundamental question in the study of Neotropical biodiversity. Several biogeographic and diversification scenarios have been proposed in the literature, but there is confusion about the processes underlying each scenario, and assessing their relative contribution is not straightforward. Here, we propose to refine these scenarios into a framework which evaluates four evolutionary mechanisms: higher speciation rate in the Andes, lower extinction rates in the Andes, older colonization times and higher colonization rates of the Andes from adjacent areas. We apply this framework to a species-rich subtribe of Neotropical butterflies whose diversity peaks in the Andes, the Godyridina (Nymphalidae: Ithomiini). We generated a time-calibrated phylogeny of the Godyridina and fitted time-dependent diversification models. Using trait-dependent diversification models and ancestral state reconstruction methods we then compared different biogeographic scenarios. We found strong evidence that the rates of colonization into the Andes were higher than the other way round. Those colonizations and the subsequent local diversification at equal rates in the Andes and in non-Andean regions mechanically increased the species richness of Andean regions compared to that of non-Andean regions (‘species-attractor’ hypothesis). We also found support for increasing speciation rates associated with Andean lineages. Our work highlights the importance of the Andean slopes in repeatedly attracting non-Andean lineages, most likely as a result of the diversity of habitats and/or host plants. Applying this analytical framework to other clades will bring important insights into the evolutionary mechanisms underlying the most species-rich biodiversity hotspot on the planet.