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Species Boundaries, Reproduction And SPECIES BOUNDARIES, REPRODUCTION AND CONNECTIVITY PATTERNS FOR SYMPATRIC TETHYA SPECIES ON NEW ZEALAND TEMPERATE REEFS MEGAN RYAN SHAFFER A thesis submitted to the Victoria University of Wellington In fulfilment of the requirements for the degree of Doctor of Philosophy VICTORIA UNIVERSITY OF WELLINGTON Te Whare Wānanga o te Ūpoko o te Ika a Māui 2019 This thesis was conducted under the supervision of: Professor James J. Bell (Primary supervisor) & Professor Simon K. Davy (Co-supervisor) Victoria University of Wellington Wellington, New Zealand ABSTRACT Understanding the evolutionary forces that shape populations in the marine environment is critical for predicting population dynamics and dispersal patterns for marine organisms. For organisms with complex reproductive strategies, this remains a challenge. Sponges fulfil many functional roles and are important components of benthic environments in tropical, temperate and polar oceans. They have evolved diverse reproductive strategies, reproducing both sexually and asexually, and thus provide an opportunity to investigate complicated evolutionary questions. This PhD thesis examines sexual and asexual reproduction in two common golf-ball sponges in central New Zealand (Tethya bergquistae and T. burtoni), with particular focus on how the environment influeunces these modes of reproduction, and further, how they shape species delineations and connectivity patterns. New Zealand waters are projected to experience increases in temperature and decreases in nutrients over the next century, and therefore these species may be experience changes in basic organismal processes like reproduction due to climate change, requiring adaptation to local environments. Therefore, this work has important implications when considering how reproductive phenology, genetic diversity and population structure of marine populations may change with shifts in climate. In my first data chapter, I highlight the difficulty in delineating sponge species by investigating the evolutionary relationship of Tethya spp. in central New Zealand using both morphological and molecular methods. Phylogenetic reconstructions based on two mitochondrial markers (rnl, COI-ext) and one nuclear marker (18S) revealed three genetic clades, with one clade representing T. bergquistae and two clades belonging to what was a priori thought to be a single species, T. burtoni. Morphological analysis based on spicule characteristics allowed T. bergquistae to be distinguished from T. burtoni, but revealed no apparent differences between the T. burtoni clades. These results indicate hidden genetic diversity within T. burtoni, which likely represents a group consisting of incipient species that have undergone speciation but have yet to express clear morphological differences. This chapter supports the notion that cryptic speciation in sponges may go undetected and diversity underestimated when using only morphology-based taxonomy, a result which has implications for conservation and management of marine systems. 5 In my second data chapter, I characterize the reproductive biology for both species of Tethya in relation to potential environmental drivers, including sea surface temperature, chlorophyll- a concentration and rainfall. Using histological methods for sponges collected monthly over two years, Tethya spp. were found to be gonochoristic and oviparous sexual reproducers, with one annual reproductive event occurring in the austral summer from January to March. Differences in oocyte density and reproductive output between both species and sites highlighted both species-specific adaptive responses and environmental influences on reproduction. Temperature and rainfall were found to be correlated with instances of sexual reproduction, and the summer reproductive event occurred each year following the spring bloom of chlorophyll-a. These findings indicate that seasonal fluctuations in the environment may be important for triggering gametogenesis for these species. With shifts in temperature, productivity, and timing of seasons projected for New Zealand, there is a potential for reproductive phenology to become mismatched with the surrounding environment under future climate change scenarios, which has consequences for the frequency, duration and overall output of sexual reproduction for these sponges. My third data chapter characterizes asexual reproduction in both species of Tethya, exploring relationships between reproductive traits and potential environmental drivers that may influence asexual budding events. Two sponge populations, one for each species of Tethya, were monitored over two years by both monthly sampling and periodic in situ observations. Data revealed that budding occurred continuously throughout the year, but had a cyclic pattern where instances of budding and densities of buds were higher during the austral spring and summer. Asexual reproduction coincided with sexual reproduction, and some individuals were found to simultaneously reproduce using both modes. Instances of asexual reproduction were positively associated with temperature and rainfall, but distinct differences between species were difficult to identify. As temperature proved important, an experiment looking at bud production in relation to thermal stress was conducted, where sponges were subjected to stable temperatures treatments of 17°C (control), 19°C and 21°C. No instances of budding were observed under any temperature treatment, and high mortality occurred in the 21°C treatment. These results suggest that temperature changes (i.e., heterogeneous environments) may be more important than temperature alone in driving asexual reproduction, and further, indicate thermal stress will result in increased sponge mortality. Correlations to potential environmental drivers indicate that future shifts in climate may affect instances of asexual reproduction and 6 thus sponge abundance, which has the potential to alter the genetic structure and overall diversity of these populations. In the final data chapter, I developed novel microsatellite markers for Tethya burtoni to characterize the genetic connectivity patterns among four populations in central New Zealand, with particular interest in the roles that sexual and asexual reproduction play in connectivity. I sampled three sites within 10 km of each other in the Wellington Region (WR), and another site on an island (Kapiti Island) approximately 50 km north of the WR. At one of the WR sample sites, I monitored a T. burtoni population over two years to examine the dispersal range of asexually reproduced buds and the ability of clones to sexually reproduce. The WR and Kapiti Island populations were strongly genetically differentiated, but within the WR region, two populations were genetically similar, indicative of high connectivity. For the monitored population, asexual bud dispersal was restricted to no greater than 1 m and clonal individuals had reduced sexual reproductive ability. Asexual reproduction did not appear to play an important role in interpopulation connectivity nor gene flow, as buds had low dispersal ability and rarely reproduced. Population structure and connectivity for T. burtoni appear to be largely driven by sexual reproduction, and asexual reproduction instead aids genotype survivorship and population maintenance. These findings highlight that different reproductive modes can differentially contribute to population dynamics in sessile marine organisms, suggesting that predictions about future population viability under changing environments may be difficult to make. In summary, this PhD thesis uses a combination of genetic, histological, field-based and experimental methods to examine species boundaries, reproduction and connectivity for Tethya spp. on rocky reefs of New Zealand. The sympatric nature, complex reproductive ecology and connectivity patterns observed likely shape the complex evolutionary processes occurring in these sponges, including introgressive hybridization and cryptic species. Individuals that showed evidence of possible introgressive events occurred mainly in populations with more restricted gene flow, while the presence of both cryptic species were more prevalent in well connected populations. Such a trend allows for discussion of under what circumstances both of these processes occur. Furthermore, environmental correlates to both sexual and asexual reproduction indicate that both of these modes of reproduction have the potential to be altered 7 with future changes in the environment. As both modes were found to play different roles in gene flow within and between populations, future shifts in climate are also expected to alter population structure and connectivity for these sponges. Such shifts in gene flow will also likely result in changes to species boundaries and thus the overall diversity of this genus. Many other sessile, benthic marine organisms present reproductive traits and behaviours similar to those of Tethya spp., and therefore these results can aid in the interpretation of results for other marine taxa. Overall, this thesis describes the population dynamics of Tethya spp., which are abundant and ecologically important on New Zealand reefs, and provides insight on how temperate sponge populations may fare with climate change, which has important implications for management and conservation efforts. 8 This thesis is dedicated to my loving and supportive parents, Jim and Peggy Shaffer. ACKNOWLEDGEMENTS To begin, I firstly need to thank James for his excellent
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