Mesoamerica is a cradle and the Atlantic Forest is a museum of Neotropical butterfly diversity: Insights from the evolution and biogeography of Brassolini (Lepidoptera: Nymphalidae)

Abstract

Regional species diversity is ultimately explained by speciation, extinction, and dispersal. Here we estimate dispersal and speciation rates in Neotropical rainforest biomes to propose an explanation for the distribution and diversity of extant butterfly species. We focus on the tribe Brassolini (owl butterflies and allies): a Neotropical group that comprises 17 genera and 108 species, most of them endemic to rainforest biomes. We infer a total-evidence species tree using the multispecies coalescent framework. By applying biogeographical stochastic mapping, we infer ancestral ranges and estimate rates of dispersal and cladogenesis at the scale of millions of years. We suggest that speciation in Mesoamerica and the northwestern flank of the Andes have only increased within the past 2 million years. In contrast, speciation in the Brazilian Atlantic Forest has been constant throughout the past 10 million years. The disparate species diversification dynamics may be partly explained by the geological and environmental history of each bioregion. Importantly, the dispersal rates into the Atlantic Forest and Mesoamerica plus NW Andes increased simultaneously in the middle-Miocene, suggesting that lineages from such regions have had comparable times for speciation despite their decoupled diversification dynamics. Diversification of extant Amazonian lineages, on the other hand, has episodically increased since the late Miocene, including a rise in speciation rate during the Pleistocene. Altogether, our results reveal a mosaic of biome-specific evolutionary histories within the Neotropics, where species have diversified rapidly (cradles: e.g., Mesoamerica), have accumulated gradually (museums: e.g., Atlantic Forest), or have alternately diversified and accumulated (e.g., Amazonia).

A diversification relay race from Caribbean-Mesoamerica to the Andes: historical biogeography of Xylophanes hawkmoths

“…A Caribbean-Mesoamerica origin is unusual among Neotropical Lepidoptera, as previous research generally recover origins in either the historically stable Amazonia or the dynamic orogeny of the Andes (e.g. [2,60] but see [10,61,62]). Our results show that Caribbean-Mesoamerica is the largest source (figure 2; electronic supplementary material, appendix S7), and the cradle (during the first phase) for Xylophanes (figure 4).…”

“…The Neotropics is one of the most species-rich regions on Earth [1]. Biodiversity studies in the Neotropics have hypothesized both the Andes and Caribbean-Mesoamerica as cradle(s) for Neotropical lineages, but only a few studies have investigated the dynamics and interactions between bioregions [1,2]. The uplift of the Andes was a major event in the geological history of South America, providing barriers and opportunities for allopatric speciation and new ecological conditions for adaption and ecological speciation of animals (e.g.…”

“…The uplift of the Andes was a major event in the geological history of South America, providing barriers and opportunities for allopatric speciation and new ecological conditions for adaption and ecological speciation of animals (e.g. [2–4]) and flora (e.g. [5,6]).…”

Hide-and-Seek with Tiny Neotenic Beetles in One of the Hottest Biodiversity Hotspots: Towards an Understanding of the Real Diversity of Jurasaidae (Coleoptera: Elateroidea) in the Brazilian Atlantic Forest

“…The Atlantic Forest is one of the Earth’s most endangered biodiversity hotspots, with less than 20% of its original cover remaining. Despite all of this loss, remaining forest fragments harbor exceptionally diverse fauna and flora with extremely high levels of speciation and endemism on the one hand, and the persistence of old lineages via low species extinction rates on the other hand, which makes this biome both a cradle and a museum of Neotropical diversity [ 31 , 33 , 63 ]. Many interesting insects were reported from the Atlantic Forest, including the bioluminescent larvae of Keroplatidae fungus gnats (Diptera) [ 64 ] and rove beetles (Staphylinidae) [ 65 ], the first Neotropical meropeid Mecoptera [ 66 ], ant-brood parasitizing scuttle flies (Phoridae) [ 67 ], and many others.…”

Biogeography of curimatid fishes reveals multiple lowland–upland river transitions and differential diversification in the Neotropics (Teleostei, Curimatidae)

“…Conversely, an evolutionary cradle is a region of net species overproduction, in which regional speciation rates exceed extinction rates, resulting in an increase of species richness and biogeographic range expansion ( i.e ., dispersal) to adjacent regions (Figure 1 ) (Albert et al, 2011 ; Rangel et al, 2018 ; Stebbins, 1974 ). Although these simple macroevolutionary models do not fully summarize the complexity of most biogeographic regions, the museum‐cradle paradigm is widely used in contemporary analyses of tropical diversification (Azevedo et al, 2020 ; Cássia‐Silva et al, 2020 ; Dagallier et al, 2020 ; Matos‐Maraví et al, 2019 ; Melo et al, 2021 ; Meseguer et al, 2020 ; Rangel et al, 2018 ). Some caveats that apply to these models are that the taxa of a given region are not expected to be monophyletic with respect to that of adjacent regions (Figure 1 ) (Albert et al, 2011 ) and that a region may simultaneously serve as a cradle for some taxa and a museum for others (McKenna & Farrell, 2006 ; Moreau & Bell, 2013 ).…”