Gainsford, Ashton (2016) A multi-disciplinary evaluation of the hybrid anemonefish Amphiprion leucokranos: behaviour shaping evolutionary outcomes of hybridization. PhD thesis, James Cook University.

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Abstract

Hybridization is an evolutionarily significant and common occurrence in nature. Interspecific breeding between closely related taxa challenges established phylogenies and questions what constitutes a species; where hybridization may drive rapid evolution of taxa and provide a source of evolutionary novelty to ecosystems. Despite the enhanced study of hybridization in recent time, a clear understanding of the mechanisms which initiate and maintain hybridization remains limited. Hybrid zones are ideal for testing theoretical questions regarding speciation and elucidating patterns of variation among species. For many taxa, reproductive success is skewed towards large, socially dominant individuals within groups, and reproductive traits and mating systems are expected to influence the outcomes of hybridization and gene exchange between hybridizing species. In this thesis, I addressed how ecology and behaviour contribute to maintenance and persistence of the Amphiprion leucokranos hybrid zone. This research employed a combination of ecological, phylogenetic and population genetic assays, as well as an observational study and behavioural experiment to test key concepts of the importance of hybridization to evolution of species.

A suite of 42 novel and published microsatellite markers were developed and tested in Chapter 2 to facilitate investigation into the relatedness of taxa within the hybrid zone. The influence of ecology and behaviour on the outcomes of hybridization were tested in Chapter 3, addressing how habitat use and relative size differences of parent species and hybrids drive patterns of gene exchange. Findings confirmed A. leucokranos to be the hybrid of closely related A. chrysopterus and A. sandaracinos, and subsequently verified that behavioural isolation, habitat use and species-specific size differences dictates the direction and degree of back-crossing and subsequent introgression. Hybridization took place exclusively with A. chrysopterus in the dominant female rank and the smaller A. sandaracinos in the sub-dominant male rank, based on mtDNA cytochrome b and multiple nDNA microsatellite loci. Overlap in habitat, depth and host anemone use was found, with hybrids intermediate to parents and co-habitation in over 25% of anemones sampled. Hybrids, intermediate in body size, colour and pattern, were classified 55% of the time as morphologically first generation hybrids relative to parents, whereas 45% of hybrids were more like A. sandaracinos, suggesting back-crossing. Unidirectional introgression of A. chrysopterus mtDNA into A. sandaracinos via hybrid back-crosses was found, with larger female hybrids and small male A. sandaracinos mating. Chapter 4 elucidated the mechanisms driving and maintaining hybridization through investigating whether social and ecological factors facilitating hybridization varied across the hybrid zone, and if this influenced gene flow and introgression regionally. Findings revealed that the relative frequency and size disparities of parent species drive regional ecological patterns and gene flow among taxa, where species integrity is maintained despite extensive mixed species group cohabitation and back-crossing. Conspecific groups were most common in Kimbe Bay (65%) where parent species relative frequency was similar. Mixed species groups dominated the Solomon Islands (82%), with larger A. chrysopterus found over 1.5 times more often than smaller A. sandaracinos. Hybrid phenotypes were highly variable across the hybrid zone, reflecting extensive back-crossing among hybrids and parent species relative to region. nDNA microsatellites defined two genetic clusters in the hybrid zone that represent parent species, despite ongoing back-crossing. Pure parent species size and relative frequency explained the existing genetic structure throughout the hybrid zone, again reflecting the characteristic size-based dominance behaviour of anemonefish. Subsequently, hybrids were directly compared to pure species when queuing within mixed groups for reproductive breeding positions in Chapter 5, addressing a significant gap in hybridization studies where hybrid inferiority is often assumed. Here, the persistence of species barriers in the face of hybridization and backcrossing was investigated, and it was demonstrated that hybrids are not always inferior to pure species, particularly when a predetermined factor such as maximum size influences dominance within a group. Hybrids positively changed rank faster and held dominant ranks more often than the smaller parent species, A. sandaracinos, indicating a fitness advantage to hybrids in the context of size-based hierarchical anemonefish breeding queues. Ultimately, hybrid only groups displayed courting behaviours associated with reproduction just as early and frequently as pure parent species. Finally, the finding of 'queue jumping' by larger A. chrysopterus highlighted the significance of abundance disparities and relative size differences to this hybridization event. This novel mechanism appears to have provided a fitness opportunity for one hybridizing taxon and may be the mechanism which originally facilitated hybridization between A. chrysopterus and A. sandaracinos.

This thesis represents an important contribution to our understanding of how hybridization persists through time and provides insight into the ecological and evolutionary outcomes for hybridizing taxa. Overall, this research highlights the importance of ecology and behaviour to the consequences of hybridization, driving patterns of gene flow and introgression across the hybrid zone. Findings suggest the coral reef fish hybrid A. leucokranos may differentiate from pure parent taxa in time, emphasizing the importance of protection for hybrids that may contribute to the biodiversity of coral reef systems. Despite challenging established phylogenies and fundamental ideas of the purity of 'true species', hybridization may hold value in conserving biodiversity, particularly on coral reefs in global decline. Conservation management must consider evolutionary theory and legislate for the protection of hybrid taxa on a case-by-case basis to effectively manage future biodiversity challenges in a changing climate.

Item ID:	52640
Item Type:	Thesis (PhD)
Keywords:	amphiprion leucokranos, anemonefish, asymmetric behavioural isolation, hybridization, hybrids, reproductive barrier, size-based hierarchy, unidirectional introgression
Related URLs:	https://researchonline.jcu.edu.au/37649/
Additional Information:	For this thesis, Ashton Gainsford received the Dean's Award for Excellence 2018. Publications arising from this thesis are available from the Related URLs field. The publications are: Chapter 3: Gainsford, A., Van Herwerden, L., and Jones, G.P. (2015) Hierarchical behaviour, habitat use and species size differences shape evolutionary outcomes of hybridization in a coral reef fish. Journal of Evolutionary Biology, 28 (1). pp. 205-222.
Date Deposited:	22 Feb 2018 01:59
FoR Codes:	06 BIOLOGICAL SCIENCES > 0604 Genetics > 060411 Population, Ecological and Evolutionary Genetics @ 34% 06 BIOLOGICAL SCIENCES > 0603 Evolutionary Biology > 060302 Biogeography and Phylogeography @ 33% 06 BIOLOGICAL SCIENCES > 0602 Ecology > 060201 Behavioural Ecology @ 33%
SEO Codes:	96 ENVIRONMENT > 9608 Flora, Fauna and Biodiversity > 960808 Marine Flora, Fauna and Biodiversity @ 50% 96 ENVIRONMENT > 9608 Flora, Fauna and Biodiversity > 960805 Flora, Fauna and Biodiversity at Regional or Larger Scales @ 50%
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