Abstract
The evolutionary success of insects has been largely attributed to the evolution of flight, yet secondary losses of flight ability have occurred in nearly all winged insect orders. One of the earliest explanations for the evolution of insect flightlessness proposed by Darwin (1859) – that strong winds select against flying individuals – has received little empirical attention. Insects that exhibit genetic wing polymorphisms, wherein both flight-capable and flightless forms co-occur, provide ideal model systems to evaluate the selection pressures acting on flight ability within populations. In this thesis, I evaluate a potential wing polymorphism in the fully winged stonefly Zelandoperla denticulata (Plecoptera: Gripopterygidae) and investigate the evolutionary maintenance of a known wing polymorphism in stoneflies from the Zelandoperla fenestrata species complex. Wing-reduced individuals related to Z. denticulata were found to represent a genetically distinct monomorphic species, which is formally described here as Zelandoperla maungatuaensis. I then applied geographical cline analyses to evaluate whether exposure above the treeline of alpine environments is associated with shifts to flightlessness in wing-polymorphic populations of the Z. fenestrata species complex. By surveying flight-capable and flightless phenotypes at sites that vary in treeline elevation (caused by deforestation), coincident losses of flight ability were revealed that were tightly linked to the treeline position of each site rather than to elevation. These results provide support for Darwin’s wind exposure hypothesis in an alpine context, and additionally provide a novel example of human-driven evolution in response to widespread clearing of native forest in New Zealand.
In fully winged populations of the Z. fenestrata species complex colour-polymorphic populations also occur. Highly melanised (black) individuals in these populations have been suggested to mimic the aposematic colouration of a chemically defended stonefly, Austroperla cyrene (Austroperlidae). The type of mimicry exhibited by Zelandoperla populations and the evolutionary origins of aposematism within the family Austroperlidae remain unclear. In this component of the thesis, I review evidence for aposematism across all known species of Austroperlidae and characterise the evolutionary and genetic basis of mimicry in a colour-polymorphic Zelandoperla population. A synthesis of taxonomic species descriptions, predator feeding studies, and dietary studies suggest that aposematism is a more widespread phenomenon within Austroperlidae than previously thought and is probably linked with dietary specialisation on wood and plant material containing compounds co-opted for defence against predators. Analyses of colouration in the Z. fenestrata species complex and A. cyrene support substantial convergence in melanism and warning signals, and controlled predation experiments demonstrate that mimetic Zelandoperla are significantly more palatable to predators than A. cyrene, consistent with Batesian mimicry. Genome-wide association analyses revealed a large-effect mutation in the gene ebony that is strongly associated with levels of melanisation in mimetic populations. Although further assessment of causal genetic variants is needed, these findings from a hemimetabolous, paleopteran order highlight the conserved role of the insect melanin biosynthesis pathway – best known in Drosophila – in the pigmentation of diverse insects. Overall, this thesis provides a foundation for future research into the evolutionary and genetic mechanisms underlying flight loss and melanism in this promising polymorphic model system.