Genetic and phenotypic evolution of the critically endangered Lord Howe Island stick insect, Dryococelus australis (Montrouzier, 1855), in captivity
Creators: name: Stuart, Oliver
Publisher: name: The Australian National University
Year: 2024

description: NB: ABSTRACT ABRIDGED TO FIT EFORM REQUIREMENTS. FOR FULL ABSTRACT SEE THESIS DOCUMENT. Captive breeding of animals is integral to human society. However, the genetic consequences of captivity can erode individual fitness. An explicit consideration of the genetic evolutionary processes at work in captive breeding programs underpins their continued success, especially as these programs expand in the 21st century as more and more populations and species are threatened by the expansion of human activity. The Lord Howe Island stick insect, Dryococelus australis (Montrouzier, 1855), is a critically endangered insect currently found in the wild only on one small island in the Pacific, Ball's Pyramid. The species is bred in captivity at the Melbourne Zoo in Melbourne, Australia, and eventually the species will be reintroduced to Lord Howe Island. The entirety of the captive population is descended from just four individuals collected in 2003. Fitness declines in captivity, detected early on the program's history, have been attributed to inbreeding. To date, no detailed genetic investigation has been undertaken. In this thesis, I present four studies, three major and one minor, on the genetics of D. australis in captivity. In Chapter 1, I examine phenotypic records from the D. australis captive breeding program, and show that individual fitness has declined over time in captivity. Then, by comparing egg hatching success over time in two captive lines, one descended only from the original founders and one hybrid line with more recent wild ancestry, I show that inbreeding depression is the likely culprit for this fitness decline. This study highlights the benefits of novel genetic material to captive breeding programs. In Chapter 2, I present a chromosome-scale genome assembly for D. australis which is used in Chapters 3 and 4. In Chapter 3, I analyse genetic diversity in the wild and in captivity using whole-genome sequence data. I document the clear effect of the captivity bottleneck on both genome-wide diversity and individual inbreeding. Hybrid individuals have diversity and inbreeding coefficients intermediate between wild individuals and captive individuals. By comparing allele frequencies between wild, hybrid, and captive individuals, I further show that strongly deleterious alleles were purged by inbreeding even through the extreme captivity bottleneck experienced by D. australis. My results show that strongly deleterious alleles are still visible to selection, even when drift is extremely strong. Finally, in Chapter 4, I use targeted resequencing to reconstruct the pedigree of a controlled D. australis breeding experiment even though most offspring were produced by asexual and not sexual reproduction. I use simulations to show that the accuracy of pedigree reconstruction depends on the overall rate of asexual reproduction where a population has a mixed reproductive mode. Mixed reproductive mode is rarely, if ever, explicitly considered by methods that aim to reconstruct familial relationships with genotype data. This study demonstrates that existing approaches may be robust to this ignorance, and that full pedigree reconstruction is possible even if a population employs occasional asexual reproduction. This thesis casts D. australis as a model for several biologically interesting processes: inbreeding depression, purging, mixed reproductive mode, and more. Moreover, it provides a detailed overview of the genetic status of D. australis, which will be crucial in guiding the management of the species in captivity and in the wild.