Understanding broad patterns of biodiversity requires developing a unified and rigorously tested theory that explains how species coexist despite the risk of competitive exclusion. Species interactions are fundamentally shaped by environmental variability. Recent theoretical development has predicted a set of general mechanisms that promote species coexistence under variable environments. Nevertheless, this theoretical framework has received limited empirical tests. Biological invasions offer excellent opportunities to empirically test coexistence mechanisms in communities in which the stability of coexistence is likely affected by introduced species. I took this opportunity to directly test the theory of species coexistence in this dissertation work by investigating how environmental variability affected the invasion of introduced species and their coexistence with native species. My collaborators and I started the investigation of diversity maintenance by first examining the range expansion of introduced species. Studying range shifts can reveal drivers of diversity patterns, which are formed by overlapping ranges of different species. We used a novel spatial analysis to determine the scale-dependent expansion rate of an invasive winter annual species, Brassica tournefortii over North America as well as to infer the drivers of this scale dependency. We found that this species expanded rapidly on scales from 5 to 500 km historically but had ceased its current expansion on the 100-500 km scales due to climatic constraints. This finding left open the question why this species continued its spread on the 5-50 km scales and how it would impact native species within its invaded range. To address these questions, we examined relatively local scale interactions between B. tournefortii and its competitors. We compared key demographic rates of B. tournefortii with other invasive and native winter annuals over a Sonoran Desert landscape to check conditions necessary for their spatial and temporal niche differentiation. We found the presence of two essential requirements for their niche differentiation: species-specific germination responses that could differentiate species by their favored environments and buffered population growth in time and space that could prevent catastrophic population declines when species faced unfavorable conditions. These conditions could provide niche opportunities to promote both the establishment of B. tournefortii and the persistence of native species under its presence. Building upon this finding, we directly quantified one general mechanism of spatial niche differentiation between B. tournefortii and its native competitors. We measured the strength of this mechanism, the spatial storage effect, across a hierarchy of spatial scales (subhabitat -> habitat -> landscape). We found that this mechanism did not promote species coexistence on any of these scales over the study period. These species were not differentiated over their tested spatial niches because weak competition following dry growing conditions failed to intensify intraspecific competition relative to interspecific competition. The strength of this mechanism increased from occasionally producing negative effects on lower scales to consistently being non-negative on the highest scale. This scale-dependent pattern was in line with the expectation that coexistence potential would increase with scales as species interacted over a wider range of environmental heterogeneity. Our findings demonstrated empirically that environmental variability in time and space led to scale-dependent patterns of the coexistence potential between introduced and native species. This work showed that introduced and native species could be differentiated by their environmental responses given spatial and temporal environmental heterogeneity on higher scales. However, for those species to stably coexist on higher scales, competitive effects had to follow environmental responses to separate species by their own density-dependent feedback loops. This work is among the first few empirical tests of a body of theory that holds the promise to generalize the mechanisms of spatial and temporal niche differentiation. Its success and limitation can motivate more studies to adopt the guiding mathematical principles and to use similar yet more innovative approaches to address the grand question of biodiversity maintenance.

Human populations evolved throughout the Old World for over 1 million years. However, anatomical characteristics of modern humans are thought to have evolved only in Africa in the last 200 thousand years. To this day, the extent to which archaic human populations contributed to the modern human gene pool is largely unknown. This work explores the evidence of genetic contribution from archaic populations at two loci in chromosome 12. Two different archaic humans, Neandertal and Denisova, living respectively in West Eurasia and in East Asia, have been indicated as potential contributors to anatomically modern human populations outside of Africa. This research shows the presence in non-Africans of two distinct introgressive alleles from archaic populations at the immune genes OAS1 and STAT2. In addition to the detection of patterns of genetic variation previously proposed as indicators of genetic introgression from archaic populations, it was possible to use the sequence of archaic individuals to infer a recent common ancestry between the introgressive modern allele and the archaic sequences. The analysis of genetic variation at the genomic region containing the gene STAT2 shows the presence of introgressive Neandertal-like and Denisova-like haplotypes. The elevated frequency in Melanesian populations of the haplotype introgressive from Neandertals suggests that this haplotype has been adaptive in Melanesians (APPENDIX B). A haplotype of the gene OAS1, nearly restricted to Melanesian populations, provides evidence of introgression from a population with genetic affinities to Denisova. The introgressive haplotype carries non-synonymous variants predicted to have functional significance and a block of very deep divergence with the remaining modern sequences (APPENDIX A). A second haplotype, observed mostly in Eurasian populations, shows evidence of having introgressed recently from Neandertals. The Neandertal-like haplotype also contains a block with very deep divergence with the remaining modern sequences (APPENDIX C). Blocks of very deep divergence within introgressive haplotypes suggest an important role of ancient population structure in the evolution of humans.

The origin of new coding sequence is a major puzzle in biology. The evolutionary pressures on new sequences are largely unknown, but structural constraints are thought to play a role. Previously, 3' untranslated region (UTR) conversion to open reading frame (ORF) was observed in Saccharomyces. We sought to identify genes that were polymorphic for stop codon position in S. cerevisiae and S. paradoxus. Using strain sequence data from the Saccharomyces Genome Resequencing Project, we found 1336 genes that had evidence of stop codon polymorphism. Of those, we found 62 genes that had evidence of addition to ancestral sequence that represented the conversion of ancestral 3' UTR to derived ORF. Two of these genes, YGL058W and YNL034W-A, are prime candidates for structural studies as they are short proteins with long additions and known structures. In future studies, they will be used to infer any structural constraints on newly evolving proteins.

I studied the insect seed predator community on mesquite plants (Prosopis spp.) to investigate patterns of community composition in space and time, attempting to better understand the factors that led to the coexistence of many seed predator species on a single plant. This dissertation begins by testing the controversial species limits of Prosopis section Algarobía because hosts may act as environmental filters to insect seed predators. I found evidence for at least eight North American Prosopis species (section Algarobía). Second, I describe and add to the known natural history of 113 arthropod species among 315,174 individuals I collected from seedpod samples across the United States and Mexico. These samples included 187 trees from eight North American Prosopis species from section Algarobía and three from section Strombocarpa. Third, I examined reproductive timing in Prosopis and show that neighboring trees of the same species reproduce synchronously, whereas closely related species stagger reproduction. I found that photoperiod is the main cue that initiates flowering, but that multiple cues are involved. Thus, synchronous reproduction may act as an equalizing process that facilitates coexistence of seed predators in this system. Fourth, I tested for evidence of spatial and temporal niche partitioning among Prosopis seed predators. I found that the rank abundance of seed predators varies little over space and time, suggesting that this community exists in a homogeneous competitive environment. I also found that although a few species restrict the use of seeds to particular host plants or developmental stages of the pods, there is little evidence of niche partitioning. Finally, I looked for evidence of competition between seed predators and examined a number of factors that may allow for coexistence of these species. I found no evidence of interspecific competition or facilitation, suggesting that species somehow either avoid competition or that present patterns are the product of past competitive interactions. Natural enemies occur too sporadically to allow for apparent competition and I found no relationship between their occurrence or abundance and those of the seed predator species I studied. I found a positive correlation between rank abundance ability and fecundity, inconsistent with expectations of life-history or competitive-colonization trade-offs. Therefore, the only stabilizing process consistent with patterns found in this system is the niche regeneration hypothesis. I found that one seed predator species lays eggs most often away from both interspecific and intraspecific competitors, a pattern consistent with active avoidance as a second equalizing process within this system.

Retroviruses infect a wide range of vertebrates. The understanding of the deep history and host distribution of retroviruses remains far from complete. Retroviruses can be integrated into their host genomes and occasionally become vertically inherited genomic loci. These integrated retroviruses, known as endogenous retroviruses (ERVs), provide "molecular fossils" for past retroviral infections and are useful for studying the deep history and ecology of retroviruses. ERVs are highly abundant in vertebrate genomes. However, endogenous foamy viruses and lentiviruses appear to be extremely rare. The primary focus of the research presented here is to discover and analyze novel endogenous foamy viruses and lentiviruses in animal genomes. Foamy virus has been thought to exclusively infect three placental mammal superorders (Laurasiatheria, Euarchontoglires, and Xenarthra). The discovery of endogenous foamy viral elements (CoeEFV) in the genome of the coelacanth (Latimeria chalumnae) extends the host range of foamy viruses to fish lineages (Appendix A). I demonstrate that foamy viruses have likely codiverged with their vertebrate hosts for more than 407 million years. The discovery of CoeEFV provides evidence for an ancient marine origin of retroviruses. Endogenous foamy virus-like elements (PSFVaye) were also identified within the genome of a Malagasy lemur, the aye-aye (Daubentonia madagascariensis) (Appendix B). Phylogenetic analysis shows that PSFVaye is divergent from all currently known simian foamy viruses, suggesting a potentially ancient association between foamy viruses and primate species. Another novel endogenous foamy virus (CaEFV) was identified in the genome of the Cape golden mole (Chrysochloris asiatica). The discovery of CaEFV reveals foamy virus infection in the placental mammal superorder Afrotheria and the long-term cospeciation between foamy viruses and placental mammals (Appendix C). Lentivirus has been thought to have a relatively recent origin. Endogenous lentivirus insertions (MELV) were discovered within the genomes of some species of the Weasel family (Mustelidae) (Appendix D). I verified the presence of MELV insertions in the genomes of several species of the Lutrinae and Mustelinae subfamilies but not the Martinae subfamily, which suggests that the lentiviral invasion likely occurred between 8.8 and 11.8 million years ago. Phylogenetic analysis suggests MELV might represent a novel lentiviral group. The discovery of MELV extends the host range of lentiviruses to the Caniformia. Endogenous lentiviruses (GvaELV) were also identified in the genome of the Sunda flying lemur (Galeopterus variegatus) (Appendix E). Phylogenetic analysis shows that GvaELV is a sister group of all known lentiviruses. The discovery of GvaELV might give a clue to the early evolution of lentiviral genome architecture. In summary, the discoveries and analyses of these novel ERVs provide important insights into the deep history and ecology of foamy viruses and lentiviruses as well as the retroviruses as a whole.

The principle of competitive exclusion holds that the strongest competitor for a single resource can exclude other species. Yet in many systems, more similar species appear to stably coexist than the small number of limiting resources. Understanding how and when similar species can stably coexist has taken on new urgency in managing biological invasions and their ecological impacts. Recent theoretical advances emphasize the importance of predators in determining coexistence. The effects of predators, however, can be mediated by behavioral changes induced in their prey as well as by their lethality. In this dissertation, I ask how considering multiple trophic levels changes our understanding of how a grass invasion (Pennisetum ciliare) affects species diversity and dynamics in southeastern Arizona. In considering interactions with plant consumers, and with the predators of those consumers, this research reveals more general ecological processes that determine species diversity across biological communities. I first present evidence from a grass removal experiment in the field that shows increased emergence and short-term survival of native perennial plants without grass. This is consistent with Pennisetum ciliare causing the observed concurrent decline in native plant abundance following invasion. I then present results from greenhouse and field studies consistent with that suppression of native plants being driven primarily through resource competition rather than increased rodent granivory. Granivorous rodents do not solely function as consumers, however, because they cache their harvested seeds in shallow scatter-hoards, from which seeds can germinate. Rodents thus act also as seed dispersers in a context-dependent mutualism. The primary granivores in areas invaded by Pennisetum ciliare are pocket mice (genus Chaetodipus), which have a well-studied tendency to concentrate their activity under plant cover to avoid predation by owls. Because the dense canopy of the grass may provide safer refuge, I hypothesized the pocket mice may be directly dispersing native seeds closer to the base of the invasive grass. Such a behavior could increase the competitive effect of the grass on native plant species, further driving the impacts of the invasion. By offering experimental seeds dusted in fluorescent powder and tracking where the seeds were cached, I show that rodents do preferentially cache experimental seeds under the grass. This dispersal interaction may be more general to plant interactions with seed-caching rodents across semi-arid regions that are experiencing plant invasions. Finally, I ask how the predator avoidance behavior exhibited by these rodents affects their ability to coexist with one another. Not only could their diversity affect that of the plant community, but the effects of plant invasions can cascade through other trophic levels. Theoretical understanding of how similar predator avoidance strategy alters coexistence had not yet been developed, however. Instead of a field study, therefore, I modified a general consumer-resource model with three trophic levels to ask whether avoidance behavior by the middle trophic level alters the ability of those species to coexist. I found that more effective avoidance behavior, or greater safety for less cost, increased the importance of resource partitioning in determining overall niche overlap. Lowering niche overlap between two species promotes their coexistence in the sense that their average fitness can be more different and still permit coexistence. These results provide novel understanding of behavioral modifications to population dynamics in multi-trophic coexistence theory applicable to this invasion and more broadly.

I asked whether there is female sterility in hybrid offspring of Mus musculus domesticus and M. m. musculus using two wild derived inbred strains representing each subspecies. I evaluated F1 hybrid female fertility by crossing F1 females to a tester male and comparing multiple reproductive parameters between intra-subspecific controls and inter-subspecific hybrids. Hybrid females had smaller litter size, reduced embryo survival, fewer ovulations, and fewer small follicles relative to controls. Significant variation in reproductive parameters was seen among different genotypes. Genes contributing to hybrid female infertility are polymorphic within subspecies. Differences in reproductive phenotypes in F1's of reciprocal crosses suggest that female subfertility may be due to either cyto-nuclear incompatibility or to imprinting. These findings suggest a greater complexity in hybrid sterility than has been previously appreciated and highlight the potential importance of hybrid female sterility in the early stages of speciation.

Estimates from radiocarbon-dated packrat middens indicate that the high elevation woodland communities of the Madrean Sky Islands were continuous as recently as 8,000 to 12,000 years ago. A number of population studies on a diverse collection of taxa have investigated the extent to which the Madrean Sky Island system has limited gene flow among mountain ranges. The results of several of these studies indicate that population divergences may be more ancient than the Holocene. Yarrow’s spiny lizards, Sceloporus jarrovii, were sampled from eight sites representing seven mountain ranges. The populations of S. jarrovii are host to the malarial parasite, Plasmodium chiricahuae. DNA sequences from the lizards and their malarial parasites were used to reconstruct the evolutionary relationships and estimate the ages of the populations for both host and parasite. The findings of these analyses indicate that the sky island populations of S. jarrovii have been isolated for hundreds of thousands of years and did not experience gene flow during the last woodland expansion. In contrast, the results indicate that the malarial infection occurred more recently, possibly during the Holocene woodland expansion. In addition, the prevalence of the malarial infection was compared to multiple attributes of the lizards. This analysis revealed a negative relationship between the genetic diversity of the lizard populations and the prevalence of infection. Furthermore, lizard populations with lower prevalence of infection have a lower frequency of multiclonal infections.

Positive frequency-dependent predation (FDP) has been proposed as a species coexistence mechanism and theoretical models have shown how it may function. In positive FDP a rare species receives a temporary reprieve from predation pressure allowing an increase to its population growth rate and a chance for it to recover from rarity. This study tests for frequency-dependent foraging by granivorous desert rodents on the seeds of three species of winter annual plants that grow in the Sonoran Desert. While the preference for one species is much higher than the other two, preferences for each species are higher when common than when rare showing an asymmetric form of positive FDP. This study is the first empirical test for positive FDP on winter annual plants and by granivorous desert rodents and one of few to use more than two prey species, native prey species, or asymmetrically preferred prey species.

A major challenge in plant ecology is in understanding how species strategies mediate interactions between the environment and fitness. Variation in niche strategies that affect phenological, physiological, and reproductive traits will allow species to partition resources differently in space and time, allowing for coexistence of many species and strategies within a community. How species differentially respond to variable environments will ultimately influence their population dynamics and geographic distribution. This dissertation approaches this topic from two perspectives: (a) examining the interaction between biogeography and variable demographic strategies in desert annual plants, and (b) examining the costs and benefits of contrasting reproductive strategies in co-occurring selfing and outcrossing desert annuals. Firstly, I tested the abundant center model to determine the role of range position on plant population dynamics. I examined how the geographic and climatic position of 13 desert annuals found at a common location, the Desert Laboratory at Tumamoc Hill in Tucson, Arizona, related to their demography over a 25-year time span. I found that species for which the Desert Laboratory was close to the center of their geographic range have less variable long-term survival and fecundity compared to species for which the Desert Laboratory was further from the center of their range. Secondly, I studied how related species with contrasting mating systems respond to variable environments to affect plant performance. In a three-year field study I investigated how inter-annual variation in plant reproductive phenology affects synchrony with pollinators and herbivores. Since selfing species are guaranteed to reproduce in the absence of pollinators, seasonal and annual variation in phenology resulted in less variable plant reproductive success compared to outcrossing species. Greater variation in reproduction in outcrossing species resulted from asynchrony in some years between plants and pollinators. In a greenhouse study examining the interaction between mating system and drought, I found that the physiological functioning and survival of outcrossing species was more strongly negatively affected by drought conditions, suggesting that selfing species have an advantage in more arid environments. These studies demonstrate how plant reproductive and physiological strategies can play a critical role in influencing fitness, population dynamics and geographic distribution.