Small insects, Big pattern: macroevolution of a hyperdiverse beetle radiation

Abstract

Beetles account for almost one quarter of all living species on earth. Yet, the drivers of this superradiation remain unclear. In this thesis, I explore this issue by focusing on a hyperdiverse beetle family, darkling beetles (Tenebrionidae). The sheer scale of species diversity, coupled with their expansive geographical distribution and enormous ecomorphological diversity, make darkling beetles an ideal model system to investigate diversification patterns over large temporal and spatial scales.

In Chapter 1, leveraging genomic datasets and modern analytical approaches, I start by establishing a phylogenomic backbone for the darkling beetle family, resolving long-standing issues over their deep relationships. In conjunction with a landmark-based dataset of body shape morphology, I show that the evolutionary history of darkling beetles is marked by an ancient rapid radiation, coupled with frequent ecological transitions and rapid bursts of morphological diversification. On a global scale, my analyses uncovered a notable pulse of phenotypic diversification proximal to the K/Pg mass extinction and remarkable convergence of body shape associated with ecological specialization. On a regional scale, I investigated two major Gondwanan radiations, Adeliini and the Heleine clade, revealing concerted response to historical events yet contrasting patterns of ecomorphological diversification. My findings align with the Simpsonian model of rapid adaptive evolution across the macroevolutionary landscape and highlight a significant role of ecological opportunity in driving the immense ecomorphological diversity in a hyperdiverse beetle group.

In Chapter 2, I shift my focus to the darkling beetle tribe Heleini, which was hypothesized to have adaptively radiated into a variety of ecological niches and evolved a diverse and characteristic arid-zone fauna on the Australian continent. By combining the molecular phylogeny established in Chapter 1 with a novel geometric morphometric dataset, I demonstrate the adaptive nature of the radiation and test the role of Miocene aridification in driving large explosive diversification. My results show that the Helea subclade of Heleini constitutes a continental-scale adaptive radiation and provide strong evidence that progressive aridification from 20 Ma opened ecological space that triggered their diversification. These findings highlight emerging environments, such as aridification, could drive large-scale adaptive radiation of preadapted lineages and set the stage for future investigations on the fine-scale diversification dynamics of this remarkable continental radiation.

In Chapter 3, I zoom into the lush rainforests of Australian Wet Tropics, where a flightless darkling beetle genus Apterotheca has rapidly radiated into over 50 micro-endemic species on mountain peaks. To achieve a comprehensive geographical sampling, I conducted a series of fieldwork on those treacherous mountain peaks. On the molecular front, I generated a mass-barcoding dataset for over 300 individuals and an exon-capture dataset for 169 individuals. On the morphological front, I collected linear measurements of body shape data for over 460 specimens. With these data, I reconstructed the evolutionary and biogeographic history of these beetles, highlighting an important role of habitat connectivity associated with fluctuating climates in the accumulation of mountain biodiversity. This work represents the most detailed phylogenomic study across the entire Wet Tropics region, providing extensive resources for future studies that seek to synthesize the drivers of speciation and community assembly in this World Heritage listed biodiversity hotspot.

Together, the work in this thesis highlights, from global to local scale, the distinct macroevolutionary trajectories undertaken by rapidly radiating clades, and is fundamental to improve our understanding of the heterogeneous evolutionary processes underpinning hyperdiversity. Show more