Into the Andes: multiple independent colonizations drive montane diversity in the Neotropical clearwing butterflies Godyridina

Abstract

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.

North Andean origin and diversification of the largest ithomiine butterfly genus

“…The biogeographical pattern of diversification, where the Andes play a central role, resembles those found in other Andean ithomiine genera, such as Hypomenitis 35, and to a lesser extent Napeogenes 6 and a clade of Oleria 4. These groups originated and diversified in the Northern Andes during the last 10 million years, a period during which the Northern Andes experienced different phases of intense uplift9.…”

“…In contrast with other ithomiine clades4635, little local diversification in Pteronymia occurred outside of the Northern Andes. An exception to this is the P. vestilla clade, which expanded into and partly diversified in lowland areas.…”

“…85%) and published63550518081 (ca. 15%) sequences from five gene regions to infer a molecular phylogeny (see Supplementary Table S1): the mitochondrial region spanning the mitochrondrial genes cytochrome oxidase c subunit 1, leucine transfer RNA and cytochrome oxidase c subunit 2 (CO1, tRNAleu, CO2, 2356 bp), and the nuclear genes tektin (735 bp) and Elongation Factor 1 alpha (EF1A, 1259 bp).…”

“…Commonly known as the clearwing butterflies because of the transparent wings in many species, they are well-known because of their involvement in Müllerian mimicry rings, whereby co-occurring unpalatable species converge in wing colour pattern amongst themselves, other Lepidoptera and some other insects34. Their diversity and broad distribution makes them a relevant study system to investigate patterns of spatial and temporal diversification in the Neotropics and they have previously been the focus of a number of diversification studies463536. Most ithomiine clades have been found to show a peak of species richness in the Andes37, but the biogeographic histories that have led to this pattern are surprisingly diverse.…”

“…Most ithomiine clades have been found to show a peak of species richness in the Andes37, but the biogeographic histories that have led to this pattern are surprisingly diverse. The genus Napeogenes originated in the Andes and subsequently dispersed out of the mountains into the Amazon Basin6, whereas rates of colonization into the Andes from adjacent areas were found to be higher in the subtribe Godyridina35. The genus Oleria contains two main subclades, one of which diversified mainly in lowland Amazonian forests while the other diversified almost exclusively in high elevation Andean cloud forests4.…”