Abstract
Effective management of vulnerable, threatened, and endangered species is crucial for their conservation and for preserving the ecosystems in which they reside. To achieve effective management, knowledge of the population structure, migration, life history traits, and habitat preferences of a species is required. However, some species have certain life history traits that make obtaining this information difficult, and as a result, management and conservation efforts can suffer. This body of work explores the power of applying genomic techniques to help better understand “difficult to manage” species for the benefit of their management and conservation using the pouched lampreys (Geotria: Geotriidae) as exemplars.
I first reviewed the information available for the five Southern Hemisphere lamprey species, finding it was distributed across literature spanning the last two centuries (1832–2020), and was often buried within larger general reviews of lampreys or Southern Hemisphere fisheries (CHAPTER 2). To make it easier for lamprey guardians (researchers, managers, and kaitiaki [caretakers]) to locate basic — but important — information on these species, I compiled over 100 years of information on Southern Hemisphere lampreys into a single synthetic review. I also identified three key knowledge gaps about pouched lampreys impacting management of these species. I then proceeded to address three key knowledge gaps using genomic methods that I thought would assist management of pouched lampreys.
Next, in collaboration with Māori iwi (the Indigenous people of New Zealand) and National Institute of Water and Atmospheric Research (NIWA), I completed the first comprehensive population genomics analysis of pouched lamprey within Aotearoa New Zealand using targeted gene sequencing (COI and Cyt-b) and restriction site- associated DNA sequencing (RADSeq) data mapped to a draft genome constructed for this study (CHAPTER 3). Pouched lamprey (G. australis) is a taonga (treasured) species in Aotearoa New Zealand that is facing population decline related to anthropogenic stressors and is threatened by lamprey reddening syndrome (LRS; main symptom = dermal reddening/haemorrhaging) which causes mass mortalities in pre- spawning adult lamprey. Employing thousands of genome-wide markers I revealed low levels of structure across ten sampling locations spanning the species range within Aotearoa New Zealand, implying either recent ongoing gene flow among populations or recent shared ancestry among Aotearoa New Zealand pouched lamprey. Using this information, guardians in Aotearoa New Zealand can now act in three key ways to improve the conservation of pouched lamprey; guardians can increase their LRS monitoring efforts on the North Island to discover the syndrome early if it occurs there, consider the implementation of propagation programs to maintain the population size, and maintain waterway migration corridors to sustain gene flow. This study demonstrated the utility of relatively inexpensive RADSeq genomic methods for genome development and the identification of fine-scale population structure of pouched lampreys.
Continuing to apply genomic methods, in collaboration with international researchers and Indigenous tribes, I then investigated Geotria population genomics collected from seven main locations spanning their known ranges throughout the Southern Hemisphere (CHAPTER 4). My analyses of RADSeq and targeted gene regions support the recently re-described G. macrostoma as being distinct from the more broadly distributed G. australis. In addition, I detected only subtle population structure across large geographic scales in G. australis. Historical demographic analyses suggested strong impacts of past climate perturbation. These findings demonstrated the utility of genomic methods to investigate both historical and present broad scale population structure in an elusive and widely-dispersed species.
In these previous chapters I evaluated the potential for lamprey reddening syndrome (LRS) to spread between populations based on inferences of gene flow, if LRS was due to a transmissible agent. I then turned my attention to trying to understand the cause of LRS, an often-fatal syndrome, that was previously observed in pouched lamprey individuals from the South Island of Aotearoa New Zealand (CHAPTER 5). Using total RNA sequencing (RNA-seq) and transcriptomic methods I produced a comprehensive transcriptome which I then used for differential expression and gene ontology enrichment analyses. My differential expression analyses of LRS-affected and non-affected lamprey identified potential agents of LRS. Of these, a virus appeared the most probable cause because the pathways associated with viral infections were upregulated in affected versus unaffected lamprey. My gene ontology analyses of the affected and non-affected lampreys also provided new insight into the understudied immune responses of lampreys, and demonstrated that formalin-fixed paraffin- embedded (FFPE) samples can help infer information about historical pathologies of a wildlife species. This research verifies the utility of genomic methods to investigate historical pathologies and immune responses of pouched lampreys while also demonstrating the function of a new method to improve our understanding of all wildlife species.
I then used the RNA-seq data to provide additional insight into pouched lamprey viruses and viral evolution. During my previous transcriptomic investigations of LRS, I discovered a novel corona virus in pouched lampreys. I described that virus as kanakana letovirus and used a combination of RNA-seq and data mining of published RNA sequencing data to identify a number of viruses that fell within the Letovirinae subfamily of the Coronaviridae (CHAPTER 6). Upon further phylogenetic analyses, I found that the coronavirus identified in the pouched lamprey fell within the phylogenetic diversity of bony fish letoviruses, indicative of past host switching events. This suggests that coronavirus evolution has been characterised by relatively frequent cross-species transmission, particularly in hosts that reside in aquatic habitats. Overall, this study demonstrates the utility of genomic methods to identify and understand potential pathogenic risks to a “difficult to manage” fish species, while highlighting the importance of monitoring other reservoirs for potential pathogens.
This thesis provides key information about pouched lampreys and demonstrates that genomic tools can be used to understand elusive and widely distributed fish species. In the final section of this work I discuss the utility of genomic tools for understanding “difficult to manage” species in detail and give my recommendations for improving the management and conservation of pouched lampreys and other “difficult to manage” species (CHAPTER 7). Based on my research, I recommend the application of genomic techniques for management and conservation programs of pouched lampreys and believe these methods present exciting new possibilities to increase our understanding of other “difficult” fishes.