The shaping of human diversity: filters, boundaries and transitions.

The evolution of modern humans was a complex process, involving major changes in levels of diversity through time. The fossils and stone tools that record the spatial distribution of our species in the past form the backbone of our evolutionary history, and one that allows us to explore the different processes-cultural and biological-that acted to shape the evolution of different populations in the face of major climate change. Those processes created a complex palimpsest of similarities and differences, with outcomes that were at times accelerated by sharp demographic and geographical fluctuations. The result is that the population ancestral to all modern humans did not look or behave like people alive today. This has generated questions regarding the evolution of human universal characters, as well as the nature and timing of major evolutionary events in the history of Homo sapiens The paucity of African fossils remains a serious stumbling block for exploring some of these issues. However, fossil and archaeological discoveries increasingly clarify important aspects of our past, while breakthroughs from genomics and palaeogenomics have revealed aspects of the demography of Late Quaternary Eurasian hominin groups and their interactions, as well as those between foragers and farmers. This paper explores the nature and timing of key moments in the evolution of human diversity, moments in which population collapse followed by differential expansion of groups set the conditions for transitional periods. Five transitions are identified (i) at the origins of the species, 240-200 ka; (ii) at the time of the first major expansions, 130-100 ka; (iii) during a period of dispersals, 70-50 ka; (iv) across a phase of local/regional structuring of diversity, 45-25 ka; and (v) during a phase of significant extinction of hunter-gatherer diversity and expansion of particular groups, such as farmers and later societies (the Holocene Filter), 15-0 ka.This article is part of the themed issue 'Major transitions in human evolution'.European Research Council (Grant ID: 295907 (Advanced Investigator Award))This is the final version of the article. It first appeared from Royal Society Publishing via http://dx.doi.org/10.1098/rstb.2015.022

Multiple attractors and long transients in spatially structured populations with an Allee effect

We present a discrete-time model of a spatially structured population and explore the effects of coupling when the local dynamics contain a strong Allee effect and overcompensation. While an isolated population can exhibit only bistability and essential extinction, a spatially structured population can exhibit numerous coexisting attractors. We identify mechanisms and parameter ranges that can protect the spatially structured population from essential extinction, whereas it is inevitable in the local system. In the case of weak coupling, a state where one subpopulation density lies above and the other one below the Allee threshold can prevent essential extinction. Strong coupling, on the other hand, enables both populations to persist above the Allee threshold when dynamics are (approximately) out-of-phase. In both cases, attractors have fractal basin boundaries. Outside of these parameter ranges, dispersal was not found to prevent essential extinction. We also demonstrate how spatial structure can lead to long transients of persistence before the population goes extinct.Comment: 25 pages, 9 figures, Submitted to Bulletin of Mathematical Biolog

Did Our Species Evolve in Subdivided Populations across Africa, and Why Does It Matter?

We challenge the view that our species, Homo sapiens, evolved within a single population and/or region of Africa. The chronology and physical diversity of Pleistocene human fossils suggest that morphologically varied populations pertaining to the H. sapiens clade lived throughout Africa. Similarly, the African archaeological record demonstrates the polycentric origin and persistence of regionally distinct Pleistocene material culture in a variety of paleoecological settings. Genetic studies also indicate that present-day population structure within Africa extends to deep times, paralleling a paleoenvironmental record of shifting and fractured habitable zones. We argue that these fields support an emerging view of a highly structured African prehistory that should be considered in human evolutionary inferences, prompting new interpretations, questions, and interdisciplinary research directions

Dispersal and eco-evolutionary dynamics in response to global change

nrpages: 171status: publishe

Species interactions in ephemeral patch systems: spatial, temporal, and spatio-temporal influences

This dissertation demonstrates the importance of spatial, temporal, and spatio-temporal mechanisms in influencing species interactions within ephemeral patch systems. This work extends prior theory using individual-based modeling to show that the autocorrelation of habitat can have a strong influence on plant-pollinator communities. Pollinators in plant-pollinator communities must regularly disperse to receptive plants, and in model systems often feed on ephemerally available seeds. Because the probability of a seed being eaten by a pollinator will be directly affected by the number of pollinators that visit a plant flower, the frequency at which seed-eating pollinators visit flowers has a major impact on the costs and benefits associated with the mutualism. High pollinator visitation increases per capita pollination, but also the number of seeds consumed. The number of pollinators visiting a plant is expected to increase with increasing plant density. Where plant habitat is especially dense, plant density will be high. If pollinator dispersal is limited, plants in these regions of high density will support high densities of pollinators that are able to move efficiently between plants. As a result of frequent pollinator visitation, plants with many nearby conspecific neighbors will produce disproportionately more pollinators than seeds. Because pollinators compete with non-pollinating exploiters of mutualisms, plants in these locations will also have lowered rates of exploitation. This is the case for the plant-pollinator interaction between the Sonoran Desert rock fig (Ficus petiolaris) and its wasp pollinator (Pegoscapus), wherein fig trees with a higher number of conspecific neighboring trees are visited by more foundress pollinators, produce fewer seeds, and are less likely to be exploited by non-pollinators. Because the costs, benefits, and stability of mutualisms with seed-eating pollinators are all strongly influenced by pollinator and exploiter birth rates, and because figs in particular are often a keystone resource for local frugivores, the work in this dissertation is of broad interest to ecology, evolution, and conservation. This dissertation also extends prior theory on competitors in ephemeral patch systems through the introduction of lottery models, which are used demonstrate how a temporal storage effect facilitates competitor coexistence when competitors develop within patches in overlapping generations. Conceptually unique to this work, the mechanism generating the temporal environmental variance on which coexistence relies is space itself, in the form of varying minimum between patch dispersal distance. When the minimum dispersal distance required to move from ephemeral patch to ephemeral patch changes over time, the superiority of competitors using patch resources can also change over time if they invest differently in fecundity versus dispersal ability. Given a trade-off in fecundity and dispersal ability, coexistence is predicted over a wide range of biologically realistic parameters for non-pollinating competitor fig wasps. An empirical prediction of this modeling work is that the fecundities of competitors in fig wasp communities will be negatively correlated with wasp dispersal abilities. Egg load estimates and two independent metrics of wasp dispersal ability show that non-pollinating competitors associated with F. petiolaris have negatively correlated fecundities and dispersal abilities. These results demonstrate that wasp population storage and a fecundity-dispersal ability trade-off are critical mechanisms for maintaining fig wasp diversity in at least one fig wasp community, and likely many others. And they more broadly demonstrate the importance of a fluctuating environment on species interactions and coexistence in ephemeral patch communities

Genomic and Ecological Dimensions of Malagasy Reptile and Amphibian Biodiversity

A long history of isolation coupled with complex topographic and ecological landscapes makes Madagascar ideal for exploring the historical factors that have shaped patterns of population diversity and endemism. Many species-level studies have suggested Late Quaternary climate change may have influenced population dynamics in the tropics, but Madagascar’s ecologically unique biomes or individual species properties may have driven idiosyncratic responses to these shifts. Using community-scale population genetic data I implement a hierarchical approximate Bayesian computation (hABC) approach to evaluate the degree of synchronous population expansion during glacial cycles across herpetofaunal assemblages both within and across discrete biomes and taxonomic groups. I integrate results from Bayesian model averaging to identify whether intrinsic and extrinsic conditions played a role in driving individualistic demographic change. I find that demographic responses are not uniform across groups, with more than 50% of all populations showing signal of recent expansion. Our explanatory models indicate species occupying narrow elevational ranges had a higher probability of expansion, while amphibian assemblages showed higher genetic diversity and greater departures from population neutrality. Expansion events were largely asynchronous, with coexpansion found in less than half of all populations. Humid-restricted taxa are the exception to this trend, with around 69–74% of all populations coexpanding during the start of the Last Glacial Period at around 100 kya, supporting the hypothesis of a more extensive humid forest cover for Madagascar during this time. I show that exploration of trait and habitat-specific demographic processes is crucial to understanding and protecting the exceptional biotic richness and endemism found in Madagascar. In my second chapter, I use genomic data from population level sampling across the island’s snakes within a comparative statistical phylogeographic framework to investigate patterns of population structure and pulses of simultaneous demographic shifts for Madagascar’s pseudoxyrhophiine snakes to determine if demographic histories been individualistic or synchronous relative to Pleistocene climate change. I identified 21 populations with a high probability of recent expansion and 12 with a history of population bottleneck. I conducted a hierarchical Random Forest analysis to estimate the proportion of lineages experiencing synchronous demographic dynamics and the timing of these events. For expanding populations, I recovered a strong signal of synchronous expansion in the Late Pleistocene after the Last Glacial Maximum. Contracting lineages showed evidence of temporally concordant bottlenecks before the onset of widespread anthropogenic Holocene fire disruption, indicating historical climate was more important in structuring contemporary patterns of diversity. I find little evidence of geographic, ecological or taxonomic signal in population diversity estimates or probability of expansion. These results suggest that areas that promoted demographic stability are not shared among broadly distributed taxa, and instead demographic change in these populations is primarily influenced by localized habitat features and species interactions. Demographic processes like population expansion often result in events like population divergence that ultimately influence patterns of genetic diversity and richness. In my third chapter, I investigate previously proposed and novel hypotheses that address the historical processes driving these patterns on Madagascar. The many widespread lineages present in the snake fauna of the island span multiple landscape and climatic barriers and represent an unparalleled opportunity to investigate the origins of endemic diversity on the island. Using genome-wide sampling, I test whether these hypotheses explain phylogeographic patterns across four codistributed, endemic snake lineages widely distributed throughout Madagascar. I evaluated the performance of two advanced regression techniques, Gradient Boosting Machine (GBM) and Random Forest regression (RF) to estimate the timing of lineage divergence, migration, and historical demographic parameters of four species groups to highlight spatial and temporal patterns of differentiation. I find that GBM outperforms RF, but both approaches estimate divergence times for the most recent diversification events in the Mid to Late Pleistocene, when overall rates in speciation declined across Madagascar snakes. Divergence was coupled with low migration rates for all species groups examined here. For at least two species groups, I find strong evidence that both climatic stability, historical refugia, and current environmental gradients have jointly contributed to population divergence over time. For dispersal limited organisms with parapatric and sympatric distributions, Madagascar’s complex ecographic and topographic history may have contributed to rapid differentiation following extreme community turnover following glacial cycles in the Quaternary

Movement ecology, survival, and territorial dynamics in Canada lynx (Lynx canadensis) over a cyclic population decline

Dissertation (Ph.D.) University of Alaska Fairbanks, 2023As the quintessential predator-prey cycle, research into Canada lynx (Lynx canadensis) and snowshoe hares (Lepus americanus) have led to many discoveries in population biology; however, much remains unknown about the nuances of their populations. In this dissertation, I examined the ways in which population cycles influence survival, reproduction, territoriality, and connectivity. First, I examined ways in which climate change induced shifts in fire regimes have affected lynx persistence in their current refugia. Lynx mainly sought out areas of higher hare density and lower cover, such as intermediately aged coniferous and deciduous forests. This type of forest was predicted to persist in the near future, so long as fire intervals remained higher than current levels. Secondly, I investigated how landscape connectivity varied as a function of dispersal status and survival. We found that although the landscape was physically well connected based on resident lynx, it was even more so given dispersing lynx tolerance of poor habitat. This was dampened by survival declines in dispersing lynx over the course of a population crash to a near complete loss of connectivity. Thirdly, I assessed the degree to which dispersal, reproduction, and survival patterns were consistent with those displayed by populations exhibiting a traveling wave. My results supported the hypothesized westward moving population wave, but one mediated by differential survival and spatially varying reproduction rather than directionally-biased dispersal. Additionally, these characteristics were consistent with lynx as driving a similar population wave in snowshoe hare. Finally, I applied a novel mathematical approach to parameterizing advection-diffusion equations to examine how territorial formation occurs at population highs. I found evidence for hierarchical formation of territories in available space, with boundaries defined by preferred habitat. This methodology was a considerable improvement over previous descriptive methods typically used to define territories, as evidenced by the model's ability to predict territorial annexation following sudden vacancy following harvest. These results underscore the importance of maintaining population refugia and existing physical connectivity for the duration of a population downturn, likely on wildlife refuges and national parks across the state, even as the impacts of climate change remain small in the near future.US Fish and Wildlife Service Inventory and Monitoring and Science Applications, Tetlin National Wildlife Refuge, David Burnett Dunn Memorial Endowment and Erich Follmann Memorial Student Research SupportChapter 1: Introduction -- Chapter 2: Complex seasonal patterns of habitat use by a keystone mesopredator in boreal forest landscapes shaped by fire -- Chapter 3: Functional connectivity of Canada lynx habitats in the North American boreal region -- Chapter 4: Evidence for a survival driven traveling wave of a boreal predator -- Chapter 5: Linking conspecific interactions and habitat selection through a mechanistic home range model to examine drivers of territoriality in an Arctic mesocarnivore -- Chapter 6: General conclusion

Evolution of associations between Cymothoe butterflies and their Rinorea host plants in tropical Africa

This thesis aimed to elucidate the evolutionary history of the associations between Cymothoeforest butterflies (Nymphalidae, Limenitidinae) and their Rinoreahost plants (Violaceae) in tropical Africa. Insects are by far the most diverse group of multicellular organisms on earth. Because most insect species are herbivores, understanding the evolution of interactions between herbivorous insects and their host plants is therefore crucial to comprehend global patterns in terrestrial biodiversity. The Cymothoe-Rinoreasystem is especially suitable for untangling processes shaping patterns of insect-host plant associations because of its high level of specificity (mostly monophagous) and the large number of related species involved (33 insect herbivores and 32 hosts). Obviously, any evolutionary study relies on a solid classification and taxonomy of the organisms under study. Unfortunately, however, in Cymothoeas well as Rinorea, taxonomy and classification is still partly unresolved. To improve taxonomy of Cymothoeand facilitate efficient identification of immature specimens found on Rinoreahost plants, we generated an extensive dataset of 1204 DNA barcode sequences (Chapter 2). Application of a novel taxonomic decision pipeline for integrating DNA barcodes with morphology and biogeography proved instrumental for solving taxonomic problems in Cymothoeand five taxa within Cymothoecould be confidently raised to species level. In addition, our DNA barcode data set allowed for the identification of 42 immature specimens from six different countries, significantly increasing the data on Cymothoehost plant associations. Nevertheless, our results also demonstrated that not all species of Cymothoecan be confidently delimited or identified. We hypothesize that this is probably due to incomplete lineage sorting and introgression (the latter possibly mediated through Wolbachiaendosymbionts) between recently diverged Cymothoespecies. In order to assess what are the best methods for matching DNA barcodes from recently diverged species, we compared six methods in their ability to correctly match DNA barcodes from selected published empirical data sets as well as simulated data (Chapter 3). Our results showed that, even though recently diverged species pose a significant problem for effective DNA barcoding, sensitive similarity-based and diagnostic methods can significantly improve identification performance compared with the commonly used tree-based methods. To improve classification and clarify the biogeographic history of Rinorea, we presented an updated phylogenetic tree of Rinoreawith increased taxonomic sampling, using plastid as well as nuclear DNA sequences (Chapter 5). Phylogenetic relationships inferred from nuclear DNA data were generally congruent with those based on evidence from plastid haplotypes from earlier studies of Rinoreaand helped resolve additional clades, some of which warrant further taxonomic study. Divergence time estimations indicated that Rinoreaoriginated in the Neotropics and reached Africa in the Eocene through trans-Atlantic dispersal. From Africa, Rinoreasubsequently dispersed into Asia in the Oligocene or early Miocene, and colonized Madagascar multiple times independently within a relatively recent time scale (Pliocene), suggesting that factors governing the independent colonizations of Rinoreato Madagascar may have been similar. In Chapter 4 we assessed whether differential rates of net species diversification in the African butterfly sister genera Harma(1 species) and Cymothoe(approximately 82 species) could best be explained by shifts to novel host plants (from Achariaceae to Rinorea) or by environmental factors such as changing climate. We generated the first time-calibrated species-level molecular phylogenetic tree of Harmaand Cymothoeand found that, after their divergence in the Miocene (15 Mya), net species diversification was low during the first 7 Myr. Coinciding with the onset of diversification of Cymothoein the late Miocene (around 7.5 Mya) there was a sharp and significant increase in diversification rate, suggesting a rapid radiation. This increased rate did not correlate with host plant transition from Achariaceae to Rinoreahost plants, but rather with a period of global cooling and desiccation, indicating that tropical forest fragmentation may well have driven the elevated diversification rates in Cymothoe. Finally, in Chapter 6 we integrated the time-calibrated phylogenetic evidence from Cymothoeand Rinoreapresented in chapters 4 and 5 with updated host association records from the field, with the aim to distinguish between alternative scenarios for the evolution of insect-host plant associations. Our results showed that: (i) divergences among extant Cymothoeare more recent than those among their associated Rinoreahosts, suggesting asynchronous diversification of Cymothoeherbivores onto already diversified clades within African Rinorea; (ii) phylogenetic trees of Cymothoeand their associated Rinoreahost plants are discordant and current associations between Cymothoeherbivores and their Rinoreahosts have developed primarily through a process of host shifting rather than by cospeciation; and (iii) related Cymothoetend to feed on related Rinoreahosts. Based on the available data, we propose a recent origin of Rinorea{}-feeding by Cymothoebutterflies with a single colonization of pre-existing lineages in the late Miocene. Current associations are best explained by a predominance of shifts among related plants, probably due to constraints in larval physiology and oviposition behaviour. Overall, these findings are in agreement with a growing body of substantial evidence to suggest that divergences of herbivorous insects and their host plants are asynchronous, and that evolutionary dynamics of hosts and parasites do not favour cospeciation. Insect-plant interactions are receiving increasing attention because of their importance in crop production and protection. At the same time, an increasing number of insects and plants that have evolved in separation are currently coming into contact due to human activities and climatic changes. It is therefore tempting to find implications of our findings for insect-host plant associations for agricultural systems (Chapter 7). Based on our results, one might predict that insects will only become pests of crops that are closely related to their natural host. Extrapolating our findings to an agricultural setting is difficult, however, because of the difference in selective pressures between natural and agricultural ecosystems.</p