Stochastic models for the ecology and population genetics of introduced species

The long-term success of an introduced population depends on the ecological conditions in its new environment, but is also influenced by stochasticity. This is particularly clear in the first stage of an invasion when the population is still small and either goes extinct quickly or establishes a self-sustaining population. Once established, some populations grow and spread spatially, with potential impacts on native communities and ecosystems. The role of stochasticity during these later invasion stages remains unclear. Furthermore, little is known about the population genetic and evolutionary consequences of stochastic invasion trajectories. With this dissertation, I would like to contribute to a stochastic eco-genetic theory of the entire invasion process—from the first introduction up to potential impacts. The overarching questions in this dissertation are: a) How does a population’s movement through the invasion process depend on ecological factors influencing its average growth rate? b) How does it depend on factors influencing the stochastic variability in the population dynamics? c) How much genetic diversity do introduced populations harbor on average upon reaching a certain point in the invasion process? d) To what extent can the population-genetic consequences of invasion trajectories feed back onto the population dynamics? Together with my advisors and coauthors, I have conducted four studies, each addressing two or more of these questions for specific ecological scenarios. We employ several types of stochastic models: Markov chains, Markov processes, their diffusion approximations, and coalescent-like genealogy simulations. In Chapter 1 (Wittmann et al., 2013a, appeared in Theoretical Population Biology), we focus on a factor influencing the introduced population’s average growth rate: the intensity of competition with an ecologically similar native species. Our results indicate that the expected time until the introduced species drives the native competitor to extinction is smallest for intermediate competition intensity. This phenomenon results from the opposing effects of competition intensity at different points of the invasion process: On the one hand, intense competition renders the establishment of the introduced population more difficult; on the other hand, it facilitates the later exclusion of the native species. In Chapter 1, we also investigate to what extent the native species’ extinction is accelerated if a reduction in population size entails a reduction in genetic diversity and thus a reduced ability to adapt to a changing environment. We find this eco-genetic feedback to be particularly strong at small competition intensities. In Chapter 2 (Wittmann et al., 2013b, in press at Oikos), we compare introduction regimes with the same average number of individuals introduced per time unit, but with a different temporal distribution. Relative to regimes with many small introduction events, regimes with few large introduction events generate more variability in population-size trajectories. We show that this variability helps introduced populations to overcome difficult stages in the invasion process (those with a negative average growth rate), but is disadvantageous during easy stages (those with a positive average growth rate). In the light of our results, we can reinterpret three published data sets on invasion success under different introduction regimes. In Chapters 3 and 4 (Wittmann et al., 2013c,d), we examine levels of genetic diversity in populations that have successfully overcome a strong demographic Allee effect. In this ecological scenario, the average population growth rate is negative below a certain critical population size and positive above, such that the first stage in the invasion process is difficult and the second one easy. In Chapter 3, we assume Poisson-distributed offspring numbers. We show that compared to successful populations without an Allee effect, successful Allee-effect populations are expected to harbor either more or less genetic diversity, depending on the magnitude of typical founder population sizes relative to the critical population size. Part of the explanation is that, counter-intuitively, successful Allee-effect populations escape particularly fast from the range of small population sizes where genetic drift is strongest. In Chapter 3, we also identify conditions under which the critical population size can be estimated from genetic data. In Chapter 4, we consider a range of offspring-number models leading to either more or less variability in population dynamics than the Poisson model. For a fixed founder population size, we observe that the Allee effect has a negative influence on genetic diversity for small amounts of variability, but a positive influence for large amounts of variability. We show that the differences between our various offspring-number models are so substantial that they cannot be resolved by rescaling the parameters of the Poisson model. Taken together, these results offer some general conclusions with respect to the four main questions raised above. a) How fast an introduced population completes the invasion process is mainly determined by the presence and severity of difficult stages. Therefore, an ecological change promotes invasion success if it lessens such difficult stages. b) From the perspective of the introduced population, variability is advantageous during difficult but not during easy stages of the invasion process. c) Because the strength of genetic drift depends on population size, a key to understanding the population genetic consequences of invasion trajectories is to consider how much time the population of interest spends in different population-size ranges. d) Feedbacks between a reduction in population size and a loss of genetic diversity are strongest in ecological scenarios where the population of interest spends considerable time at small population sizes. Some of the most striking results in this dissertation cannot be understood from a deterministic point of view, but only when considering stochasticity. Thus, stochasticity does not just add “noise” to some average outcome, but can qualitatively change the behavior of biological systems.Der langfristige Erfolg einer eingeführten Population hängt von den ökologischen Bedingungen in ihrer neuen Umgebung ab, aber auch vom Zufall. Besonders offensichtlich ist die wichtige Rolle des Zufalls für kleine Populationen im Anfangsstadium einer Invasion. In diesem Stadium entscheidet sich, ob die eingeführte Population nach kurzer Zeit ausstirbt oder sich dauerhaft etablieren kann. Manche etablierten Populationen wachsen dann weiter und breiten sich räumlich aus, zum Teil mit schwerwiegenden Folgen für einheimische Gemeinschaften und Ökosysteme. Bislang ist nicht klar, welche Rolle der Zufall in diesen späteren Invasionsstadien spielt und welche populationsgenetischen und evolutionären Auswirkungen vom Zufall geprägte Invasionsverläufe haben. Mit dieser Dissertation möchte ich beitragen zu einer stochastischen öko-genetischen Theorie des gesamten Invasionsprozesses – von der Einführung bis hin zu möglichen Auswirkungen. Meine übergreifenden Fragen sind: a) Welche Rolle für den Invasionsverlauf spielen ökologische Faktoren, die die durchschnittliche Wachstumsrate der eingeführten Population beeinflussen? b) Und welche Rolle spielen Faktoren, die die stochastische Variabilität der Populationsdynamik beeinflussen? c) Wie viel genetische Diversität weisen eingeführte Populationen im Durchschnitt auf, wenn sie einen bestimmten Punkt im Invasionsprozess erreichen? d) Inwiefern können die populationsgenetischen Auswirkungen von Invasionsverläufen wiederum die Populationsdynamik beeinflussen und so zu einer Rückkopplung führen? Zusammen mit meinen Betreuern und Koautoren habe ich vier Studien durchgeführt, die sich für bestimmte ökologische Szenarien jeweils mit mindestens zwei dieser Fragen befassen. Dazu kommen im Verlauf der Dissertation verschiedene Typen von stochastischen Modellen zum Einsatz: Markov-Ketten, Markov- und Diffusionsprozesse sowie Coalescent-artige Genealogie-Simulationen. In Kapitel 1 (Wittmann et al., 2013a, erschienen in Theoretical Population Biology) konzentrieren wir uns auf einen Faktor, der die durchschnittliche Wachstumsrate der Population beeinflusst: die Stärke der Konkurrenz mit einer ökologisch ähnlichen einheimischen Art. Unsere Ergebnisse deuten darauf hin, dass die erwartete Zeit bis zum Aussterben des einheimischen Konkurrenten für mittlere Konkurrenzstärken am kleinsten ist. Das können wir dadurch erklären, dass die Konkurrenzstärke gegensätzliche Auswirkungen in verschiedenen Stadien des Invasionsprozesses hat: Einerseits erschwert eine hohe Konkurrenzstärke die Etablierung der eingeführten Art, andererseits führt eine hohe Konkurrenzstärke aber auch dazu, dass die einheimische Art schnell verdrängt werden kann. Zusätzlich untersuchen wir in Kapitel 1, wie stark eine öko-genetische Rückkopplung das Aussterben der einheimischen Population beschleunigen würde. Dazu berücksichtigen wir, dass ein Rückgang der einheimischen Populationsgröße zu einem Verlust an genetischer Diversität führt, und das wiederum zu schlechterer Anpassung an veränderte Umweltbedingungen und darum weiterem Schrumpfen der Population. Unsere Ergebnisse legen nahe, dass diese öko-genetische Rückkopplung dann besonders stark ist, wenn die Konkurrenz zwischen einheimischer und eingeführter Art eher schwach ist. In Kapitel 2 (Wittmann et al., 2013b, im Druck bei Oikos) untersuchen wir für feste durchschnittliche Einführungsraten (Individuen pro Zeiteinheit), welche Rolle die zeitliche Verteilung der Individuen spielt. Besonders wichtig ist hierbei die Beziehung zwischen zeitlicher Verteilung und der Variabilität in der Größenentwicklung der Population. Wir zeigen, dass Fälle mit wenigen großen Einführungsereignissen zu mehr Variabilität führen als Fälle mit vielen kleinen Einführungsereignissen. Diese Variabilität hilft den eingeführten Populationen dabei, schwierige Stadien im Invasionsprozess (also solche mit einer negativen durchschnittlichen Wachstumsrate) zu bewältigen, ist aber anderseits in einfachen Stadien mit positiver durchschnittlicher Wachstumsrate von Nachteil. Im Lichte unserer Ergebnisse können wir aus der Literatur bekannte Daten zu Invasionsprozessen neu interpretieren. In den Kapiteln 3 und 4 (Wittmann et al., 2013c,d) untersuchen wir die genetische Diversität von Populationen, die einen starken demografischen Allee-Effekt erfolgreich überwunden haben. Laut Definition ist dabei die durchschnittliche Wachstumsrate bei Populationsgrößen unterhalb einer gewissen kritischen Größe negativ und in größeren Populationen positiv, so dass das erste Stadium des Invasionsprozesses schwierig ist und das zweite einfach. In Kapitel 3 zeigen wir unter der Annahme Poisson-verteilter Nachkommenzahlen, dass erfolgreiche Allee-Effekt-Populationen je nach Startgröße entweder eine höhere oder eine niedrigere durchschnittliche genetische Diversität aufweisen als erfolgreiche Populationen ohne Allee-Effekt. Das kommt zum Teil daher, dass erfolgreiche Allee-Effekt-Populationen besonders schnell das schwierige erste Stadium des Invasionsprozesses verlassen, wo genetische Drift am stärksten ist. Außerdem untersuchen wir in Kapitel 3, unter welchen Bedingungen sich die kritische Populationsgröße aus genetischen Daten schätzen lässt. In Kapitel 4 betrachten wir eine Reihe von Modellen für die Anzahl an Nachkommen von Individuen oder Paaren in der Population. Manche dieser Modelle führen zu mehr stochastischer Variabilität in der Populationsdynamik, andere zu weniger Variabilität als das in Kapitel 3 betrachtete Poisson-Modell. Für feste Startgröße beobachten wir, dass der Allee-Effekt bei kleiner Variabilität einen negativen Einfluss auf die genetische Diversität hat und bei großer Variabilität einen positiven Einfluss. Wir zeigen weiterhin, dass die Unterschiede zwischen unseren Nachkommenzahl-Modellen so substanziell sind, dass sie sich nicht durch eine Umskalierung der Parameter des Poisson-Modells erklären lassen. Zusammen genommen erlauben uns diese Ergebnisse einige allgemeine Schlussfolgerungen bezüglich der vier oben aufgeführten übergreifenden Fragen. a) Wie schnell eine eingeführte Population den Invasionsprozess durchläuft, hängt hauptsächlich davon ab, ob es schwierige Stadien gibt, und wie schwierig diese sind. Deshalb begünstigt eine ökologische Veränderung den Invasionserfolg dann, wenn sie schwierige Stadien im Invasionsprozess mindert. b) Aus der Perspektive der eingeführten Population ist Variabilität in schwierigen Stadien des Invasionsprozesses von Vorteil, aber in einfachen Stadien von Nachteil. c) Da die Stärke der genetischen Drift von der Populationsgröße abhängt, können wir die populationsgenetischen Auswirkungen von Invasionsverläufen verstehen, indem wir analysieren, wie viel Zeit die betrachtete Population in verschiedenen Populationsgrößenbereichen verbringt. d) Rückkopplungen zwischen einem Rückgang der Populationsgröße und einem Verlust genetischer Diversität sind am stärksten, wenn die Population viel Zeit im Bereich kleiner Populationsgrößen verbringt. Einige der wesentlichsten Ergebnisse dieser Dissertation können aus einer deterministischen Perspektive nicht verstanden werden, sondern sind ein direktes Produkt von Stochastizität. Dies macht deutlich, dass Stochastizität nicht einfach einem gewissen Durchschnitts- ergebnis etwas Rauschen hinzufügt, sondern das Verhalten biologischer Systeme qualitativ verändern kann

Ecological and genetic effects of introduced species on their native competitors

Species introductions to new habitats can cause a decline in the population size of competing native species and consequently also in their genetic diversity. We are interested in why these adverse effects are weak in some cases whereas in others the native species declines to the point of extinction. While the introduction rate and the growth rate of the introduced species in the new environment clearly have a positive relationship with invasion success and impact, the influence of competition is poorly understood. Here, we investigate how the intensity of interspecific competition influences the persistence time of a native species in the face of repeated and ongoing introductions of the nonnative species. We analyze two stochastic models: a model for the population dynamics of both species and a model that additionally includes the population genetics of the native species at a locus involved in its adaptation to a changing environment. Counterintuitively, both models predict that the persistence time of the native species is lowest for an intermediate intensity of competition. This phenomenon results from the opposing effects of competition at different stages of the invasion process: With increasing competition intensity more introduction events are needed until a new species can establish, but increasing competition also speeds up the exclusion of the native species by an established nonnative competitor. By comparing the ecological and the eco-genetic model, we detect and quantify a synergistic feedback between ecological and genetic effects.Comment: version accepted at Theoretical Population Biolog

Categorizing diffuse parenchymal lung disease in children

Background Aim of this study was to verify a systematic and practical categorization system that allows dynamic classification of pediatric DPLD irrespective of completeness of patient data. Methods The study was based on 2322 children submitted to the kids-lung-register between 1997 and 2012. Of these children 791 were assigned to 12 DPLD categories, more than 2/3 belonged to categories manifesting primarily in infancy. The work-flow of the pediatric DPLD categorization system included (i) the generation of a final working diagnosis, decision on the presence or absence of (ii) DPLD and (iii) a systemic or lung only condition, and (iv) the allocation to a category and subcategory. The validity and inter-observer dependency of this workflow was re-tested using a systematic sample of 100 cases. Results Two blinded raters allocated more than 80 % of the re-categorized cases identically. Non-identical allocation was due to lack of appreciation of all available details, insufficient knowledge of the classification rules by the raters, incomplete patient data, and shortcomings of the classification system itself. Conclusions This study provides a suitable workflow and hand-on rules for the categorization of pediatric DPLD. Potential pitfalls were identified and a foundation was laid for the development of consensus-based, international categorization guidelines

Lung disease caused by ABCA3 mutations

Background Knowledge about the clinical spectrum of lung disease caused by variations in the ATP binding cassette subfamily A member 3 (ABCA3) gene is limited. Here we describe genotype-phenotype correlations in a European cohort. Methods We retrospectively analysed baseline and outcome characteristics of 40 patients with two disease-causing ABCA3 mutations collected between 2001 and 2015. Results Of 22 homozygous (15 male) and 18 compound heterozygous patients (3 male), 37 presented with neonatal respiratory distress syndrome as term babies. At follow-up, two major phenotypes are documented: patients with (1) early lethal mutations subdivided into (1a) dying within the first 6 months or (1b) before the age of 5 years, and (2) patients with prolonged survival into childhood, adolescence or adulthood. Patients with null/null mutations predicting complete ABCA3 deficiency died within the 1st weeks to months of life, while those with null/other or other/other mutations had a more variable presentation and outcome. Treatment with exogenous surfactant, systemic steroids, hydroxychloroquine and whole lung lavages had apparent but many times transient effects in individual subjects. Conclusions Overall long-term (>5 years) survival of subjects with two disease-causing ABCA3 mutations was <20%. Response to therapies needs to be ascertained in randomised controlled trials

Post-Transcriptional Regulation of 5-Lipoxygenase mRNA Expression via Alternative Splicing and Nonsense-Mediated mRNA Decay

5-Lipoxygenase (5-LO) catalyzes the two initial steps in the biosynthesis of leukotrienes (LT), a group of inflammatory lipid mediators derived from arachidonic acid. Here, we investigated the regulation of 5-LO mRNA expression by alternative splicing and nonsense-mediated mRNA decay (NMD). In the present study, we report the identification of 2 truncated transcripts and 4 novel 5-LO splice variants containing premature termination codons (PTC). The characterization of one of the splice variants, 5-LOΔ3, revealed that it is a target for NMD since knockdown of the NMD factors UPF1, UPF2 and UPF3b in the human monocytic cell line Mono Mac 6 (MM6) altered the expression of 5-LOΔ3 mRNA up to 2-fold in a cell differentiation-dependent manner suggesting that cell differentiation alters the composition or function of the NMD complex. In contrast, the mature 5-LO mRNA transcript was not affected by UPF knockdown. Thus, the data suggest that the coupling of alternative splicing and NMD is involved in the regulation of 5-LO gene expression

Conceptual Frameworks and Methods for Advancing Invasion Ecology

Invasion ecology has much advanced since its early beginnings. Nevertheless, explanation, prediction, and management of biological invasions remain difficult. We argue that progress in invasion research can be accelerated by, first, pointing out difficulties this field is currently facing and, second, looking for measures to overcome them. We see basic and applied research in invasion ecology confronted with difficulties arising from (A) societal issues, e.g., disparate perceptions of invasive species; (B) the peculiarity of the invasion process, e.g., its complexity and context dependency; and (C) the scientific methodology, e.g., imprecise hypotheses. To overcome these difficulties, we propose three key measures: (1) a checklist for definitions to encourage explicit definitions; (2) implementation of a hierarchy of hypotheses (HoH), where general hypotheses branch into specific and precisely testable hypotheses; and (3) platforms for improved communication. These measures may significantly increase conceptual clarity and enhance communication, thus advancing invasion ecology

Modeling minimum viable population size with multiple genetic problems of small populations

Nabutanyi P, Wittmann M. Modeling minimum viable population size with multiple genetic problems of small populations. Conservation biology : the journal of the Society for Conservation Biology. 2022: e13940.An important goal for conservation is to define minimum viable population (MVP) sizes for long-term persistence of a species. There is increasing evidence of the role of genetics in population extinction; thus, conservation practitioners are starting to consider the effects of deleterious mutations (DM), in particular the effects of inbreeding depression on fitness. We sought to develop methods to account for genetic problems other than inbreeding depression in MVP estimates, quantify the effect of the interaction of multiple genetic problems on MVP sizes, and find ways to reduce the arbitrariness of time and persistence probability thresholds in MVP analyses. To do so, we developed ecoevolutionary quantitative models to track population size and levels of genetic diversity. We assumed a biallelic multilocus genome with loci under single or multiple, interacting genetic forces. We included mutation-selection-drift balance (for loci with DM) and 3 forms of balancing selection for loci for which variation is lost through genetic drift. We defined MVP size as the lowest population size that avoids an ecoevolutionary extinction vortex. For populations affected by only balancing selection, MVP size decreased rapidly as mutation rates increased. For populations affected by mutation-selection-drift balance, the MVP size increased rapidly. In addition, MVP sizes increased rapidly as the number of loci increased under the same or different selection mechanisms until even arbitrarily large populations could not survive. In the case of fixed number of loci under selection, interaction of genetic problems did not always increase MVP sizes. To further enhance understanding about interaction of genetic problems, there is need for more empirical studies to reveal how different genetic processes interact in the genome. © 2022 The Authors. Conservation Biology published by Wiley Periodicals LLC on behalf of Society for Conservation Biology

C++ source code and R scripts for Wittmann et al. (2017)

This folder contains the simulation program, summarized simulation results, and all scripts underlying the analyses and plots in Wittmann et al. (2017) Seasonally fluctuating selection can maintain polymorphism at many loci via segregation lift.<br

Eco-Evolutionary Buffering: Rapid Evolution Facilitates Regional Species Coexistence despite Local Priority Effects

Wittmann M, Fukami T. Eco-Evolutionary Buffering: Rapid Evolution Facilitates Regional Species Coexistence despite Local Priority Effects. The American Naturalist. 2018;191(6):E171-E184.Inhibitory priority effects, in which early-arriving species exclude competing species from local communities, are thought to enhance regional species diversity via community divergence. Theory suggests, however, that these same priority effects make it difficult for species to coexist in the region unless individuals are continuously supplied from an external species pool, often an unrealistic assumption. Here we develop an eco-evolutionary hypothesis to solve this conundrum. We build a metacommunity model in which local priority effects occur between two species via interspecific interference. Within each species there are two genotypes: one is more resistant to interspecific interference than the other but pays a fitness cost for its resistance. Because of this trade-off, species evolve to become less resistant as they become regionally more common. Rare species can then invade some local patches and consequently recover in regional frequency. This "eco-evolutionary buffering" enables the regional coexistence of species despite local priority effects, even in the absence of immigration from an external species pool. Our model predicts that eco-evolutionary buffering is particularly effective when local communities are small and connected by infrequent dispersal