Dissertations, Theses, and Capstone Projects

Date of Degree

9-2023

Document Type

Dissertation

Degree Name

Ph.D.

Program

Biology

Advisor

Michael J. Hickerson

Committee Members

Ana Carnaval

John P. Wares

Cheryl Hayashi

Elizabeth Alter

Subject Categories

Biodiversity | Ecology and Evolutionary Biology | Evolution | Genomics | Marine Biology | Population Biology

Keywords

population genomics, marine invertebrates, intertidal ecology, marine conservation, echinoderm

Abstract

Uncovering how species respond to environmental change is a central question in biology (Ehrlén & Morris 2015; Habibullah et al. 2022). It is the key to elucidating the past, understanding the present and predicting the future of species’ population dynamics. This dissertation investigates the influence of environmental change on intertidal species’ distributions and genomics at several timescales, with implications for conservation.

Environmental changes have occurred throughout history, on a geological scale, and have shaped the global patterns of species’ distributions and population sizes. Biologists have long studied how geological history has shaped species distributions (Sanmartín 2012) in both terrestrial (Liu et al. 2019; Musher et al. 2022) and marine systems (Addison & Hart 2005; Woodhouse et al. 2023). Ancient processes, such as glaciation patterns and climate fluctuations, can also leave signatures in species’ genomes (Miller et al. 2012; Liu et al. 2019). With recent advances in genomic sequencing, it is now possible to investigate the influence of environmental processes along the genome and across the globe, even in non-model organisms for which we have little other context (Ellegren et al. 2012; Rincon-Sandoval et al. 2019).

On a more recent timescale, genome-wide data can be used to assess the current dynamics of species. This includes local adaptation to the environment (Prates et al. 2018) and how population structure and hybridization is shaped by environmental forces (Kruuk et al. 1999; Taylor et al. 2014). In tandem with ecological modeling, such as species distribution models (SDMs), we can also assess global species distributions, and how they are influenced by these environmental factors along with genomic variation (Ehrlén & Morris 2015; Mathieu-Bégné et al. 2021; Aguirre-Liguori et al. 2021). In the face of a rapidly changing climate, we can use these methods to infer information about environmental influences on current dynamics to predict what might occur to species distributions and genomic variation in the future (Razgour et al. 2019; Waldvogel et al. 2020; Kardos et al. 2021). In some cases, this can help to mitigate the impacts of climate change by informing conservation and wildlife management (Harrisson et al. 2014; Supple & Shapiro 2018; Rellstab et al. 2021).

Studying keystone species is a particularly useful way to understand and predict the population dynamics of entire communities. A keystone species is one which has an outsized impact on the rest of their ecological community; often, these species maintain stability and diversity in a system, and their population fluctuations affect the entire species assemblage in which they reside (Paine 1966). Sea stars are known to be keystone species in the intertidal community (Paine 1966; Hart 2010; Menge & Sanford 2013), and are therefore of great interest to ecologists and conservation biologists hoping to predict and mitigate impending biodiversity loss. Despite their economic and ecological importance (Costanza et al. 1997) and evidence that marine systems will suffer greater losses in biodiversity due to climate change (Blowes et al. 2019), marine species are often less well-studied than their terrestrial counterparts and are treated as an entirely separate entity (Webb 2012). Intertidal organisms are particularly useful to study in the context of climate change as they occupy portions of both the terrestrial and marine realms, and can function as an early warning system for climate change (Helmuth et al. 2006).

This dissertation encompasses three chapters representing in-depth study of Asterias sea stars in the North Atlantic and their responses to environmental change across multiple temporal scales. Asterias are known to be keystone species in the North Atlantic rocky intertidal (Lubchenco & Menge 1978; MacKenzie & Pikanowski 1999). The climate of this region is changing rapidly (Pershing et al. 2015), and species composition is changing along with it (Petraitis & Dudgeon 2020). My research uses genomics, ecological modeling, and field surveys to study the past, current dynamics, and future of Asterias in the North Atlantic Ocean.

First, to understand what shapes current Asterias distributions and genomic variation, I use genome-wide restriction site associated DNA markers (RADseq) to identify the geographic extent of the hybrid zone between A. rubens and A. forbesi as well as the environmental forces that maintain their hybrid cline. I also use these data to identify and compare the genome-environmental associations in each species. I also use ecological niche modeling to characterize the differential use of geographic and environmental space of each species. Hybridization and geographic patterns could change along with climate, which could influence the future trajectories of these species’ distributions and ability to adapt and survive.

To elucidate how historical environmental change has impacted the genomes of Asterias, I infer their demographic history as well as genome-wide divergence, selection, and introgression by using low-coverage whole genomes from both species and their Pacific outgroup A. amurensis. This has uncovered a long history of introgression and divergence within this group, which is apparent from both my inference of population size histories as well as from the distributions of ancestry blocks throughout the genomes. These analyses also find introgression to be asymmetrical; with A. forbesi showing a greater proportion of introgressed sites than A. rubens. This chapter highlights the power of whole genomes to illuminate fine-scale genomic patterns that reduced representation genomic data is unable to discern. It also sheds light on the influence of geological history and historical climate in shaping the genomes of marine species.

In my final chapter, I document and quantify a monumental decline in Asterias in the North Atlantic and aim to understand how human-induced environmental changes have contributed to this dynamic. I replicate a seminal 1979 survey across New England, and find that Asterias density in this region has decreased by orders of magnitude (Menge 1979). These sea stars also seem to have shifted ecologically; they have moved from the intertidal to the subtidal, and small recruits now represent a smaller proportion of the population than in 1979. I also postulate several reasons for this decline, including Sea Star Wasting, invasive species, and climate change. This study has wide-ranging implications for the future of the coastal community of the North Atlantic and is of interest to wildlife managers in the region.

In summary, this dissertation advances our knowledge of how changes in the environment can shape the global distributions and genomes of species and several geographic and temporal scales. This work has implications for molecular evolution and biogeography, and by focusing on a North Atlantic intertidal keystone species, this research also has applications for conservation of a declining keystone species.

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