Palaeoenvironmental shifts drove the adaptive radiation of a noctuid stemborer tribe (Lepidoptera, Noctuidae, Apameini) in the miocene

Abstract

Between the late Oligocene and the early Miocene, climatic changes have shattered the faunal and floral communities and drove the apparition of new ecological niches. Grassland biomes began to supplant forestlands, thus favouring a large-scale ecosystem turnover. The independent adaptive radiations of several mammal lineages through the evolution of key innovations are classic examples of these changes. However, little is known concerning the evolutionary history of other herbivorous groups in relation with this modified environment. It is especially the case in phytophagous insect communities, which have been rarely studied in this context despite their ecological importance. Here, we investigate the phylogenetic and evolutionary patterns of grass-specialist moths from the species-rich tribe Apameini (Lepidoptera, Noctuidae). The molecular dating analyses carried out over the corresponding phylogenetic framework reveal an origin around 29 million years ago for the Apameini. Ancestral state reconstructions indicate (i) a potential Palaearctic origin of the tribe Apameini associated with a major dispersal event in Afrotropics for the subtribe Sesamiina; (ii) a recent colonization from Palaearctic of the New World and Oriental regions by several independent lineages; and (iii) an ancestral association of the tribe Apameini over grasses (Poaceae). Diversification analyses indicate that diversification rates have not remained constant during the evolution of the group, as underlined by a significant shift in diversification rates during the early Miocene. Interestingly, this age estimate is congruent with the development of grasslands at this time. Rather than clade ages, variations in diversification rates among genera better explain the current differences in species diversity. Our results underpin a potential adaptive radiation of these phytophagous moths with the family Poaceae in relation with the major environmental shifts that have occurred in the Miocene.

Figure 1. Phylogenetic relationships of the tribe Apameini within the superfamily Noctuoidea under Bayesian inference.

Posterior probabilities (PP) are indicated above the nodes (* indicates a value up to 0.95). When no values are indicated, it means that the PP was <0.95, except for some basal nodes for which the support is annotated. Groups of interest are highlighted by vertical bands of different colours referring to the colour of the clades. The Apameini, Sesamiina and Apameina (excluding the three genera Staurophora, Calamia and Litholomia) nodes are respectively labelled N1, N2 and N3. Names of the species for which a habitus is displayed are specified under the pictures (Pictures: EFA Toussaint & BP Le Ru).

Figure 2. Maximum credibility tree with median ages (Myr) from the Bayesian uncorrelated uniform analysis under BEAST for the superfamily Noctuoidea.

A 5 Myr-timescale is placed at the bottom of the chronogram and spans the Cretaceous to the Holocene. Brown hourglasses at the corresponding nodes indicate the calibration points used to ultrametrize the topology. For the fossil calibration, a picture of the moth in question retrieved from Douglas SD & Stockey RA (1996) is presented in the bottom left-corner. Horizontal blue bands represent the 95% HPD heights (in Myr) for the major nodes of the chronogram. Vertical bands and pastilles at the nodes of different colours referring to the colour of the clades highlight groups of interest. For the groups of major interest, the name is given in a box of the clade colour. Abbreviations for the clade names are: Ere.  =  Erebidae, Eut.  =  Euteliidae, Hel.  =  Helicoverpa, and Nol.  =  Nolidae. Genera of the Sesamiina and Apameina subtribes show respectively green and orange branches. Names of the species for which a habitus is displayed are specified under the picture (Pictures: EFA Toussaint & BP Le Ru).

Figure 3. Estimates of net diversification rates and ancestral host plant reconstruction of the tribe Apameini based on the Bayesian chronogram.

A coloured pastille indicating the most likely ancestral host plant is displayed at the root of the topology and at the nodes for which a host-plant shift (green arrow) is observed. When no pastille is shown, it means that the ancestral host plant is the same as the root. Present hot-plants are specified on the right of the genera names. Colours of the pastilles correspond to the listed families at the bottom left corner of the chronogram. Asterisks above the nodes indicate a strong support for the recovered family (>2 log-likelihood units against the second better score). A 5 Myr-timescale is placed at the bottom of the chronogram. The vertical bars next to the genera names delimit the two subtribes (Apameina in orange and Sesamiina in green). The net diversification rates calculated for each genus are shown on the branches. Colour of the branches match the different levels of rates presented above the host-plant families. Two stars at corresponding nodes indicate maximum likelihood estimate of rate-shift location inferred under two-rate diversification model. The species richness of each genus is displayed in brackets after the name. At the bottom of the figure, a graphic illustrates the variations in relative temperature (approximated by δ¹⁸O in ‰) from the mid-Oligocene to the Holocene. Major climatic events are presented along with the most important stages in the evolution of grasses.

Figure 4. Historical biogeography of the tribe Apameini reconstructed using the DEC model based on the median-BEAST chronogram.

A coloured square indicating the most likely ancestral area is displayed at each node of the topology. Colours of the squares correspond to the colour of the areas presented in the map at the bottom left corner of the chronogram. Asterisks above the nodes indicate a strong support for the recovered areas (>2 log-likelihood units against the second better score). A 5 Myr-timescale is placed at the bottom of the chronogram and goes from the mid-Oligocene to the Holocene. The vertical bars next to the genera names delimit the two subtribes (Apameina in orange and Sesamiina in green). The biogeographical scenario for the tribe is presented in two maps at the bottom of the figure. Dotted-lines above the maps specify the related epoch (Left map: Oligocene and right map: Miocene). The origin of the group is highlighted by a yellow and red symbol, and the major dispersal events are shown with arrows.