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bioRxiv2018

Using machine learning to associate bacterial taxa with functional groups through flow cytometry, 16S rRNA gene sequencing, and productivity data

High-(HNA) and low-nucleic acid (LNA) bacteria are two operational groups identified by flow cytometry (FCM) in aquatic systems. HNA cell density often correlates strongly with heterotrophic production, while LNA cell density does not. However, which taxa are specifically associated with these groups, and by extension, productivity has remained elusive. Here, we addressed this knowledge gap by using a machine learning-based variable selection approach that integrated FCM and 16S rRNA gene sequencing data collected from 14 freshwater lakes spanning a broad range in physicochemical conditions. There was a strong association between bacterial heterotrophic production and HNA absolute cell abundances (R2 = 0.65), but not with the more abundant LNA cells. This solidifies findings, mainly from marine systems, that HNA and LNA could be considered separate functional groups, the former contributing a disproportionately large share of carbon cycling. Taxa selected by the models could predict HNA and LNA absolute cell abundances at all taxonomic levels, with the highest performance at the OTU level. Selected OTUs ranged from low to high relative abundance and were mostly lake system-specific (89.5%-99.2%). A subset of selected OTUs was associated with both LNA and HNA groups (12.5%-33.3%) suggesting either phenotypic plasticity or within-OTU genetic and physiological heterogeneity. These findings may lead to the identification of systems-specific putative ecological indicators for heterotrophic productivity. Generally, our approach allows for the association of OTUs with specific functional groups in diverse ecosystems in order to improve our understanding of (microbial) biodiversity-ecosystem functioning relationships. ImportanceA major goal in microbial ecology is to understand how microbial community structure influences ecosystem functioning. Research is limited by the ability to readily culture most bacteria present in the environment and the difference in bacterial physiology in situ compared to in laboratory culture. Various methods to directly associate bacterial taxa to functional groups in the environment are being developed. In this study, we applied machine learning methods to relate taxonomic data obtained from marker gene surveys to functional groups identified by flow cytometry. This allowed us to identify the taxa that are associated with heterotrophic productivity in freshwater lakes and indicated that the key contributors were highly system-specific, regularly rare members of the community, and that some could switch between being low and high contributors. Our approach provides a promising framework to identify taxa that contribute to ecosystem functioning and can be further developed to explore microbial contributions beyond heterotrophic production.

ecology↗

bioRxiv2018

Biogeography masks diet-induced shifts in the bacterial community associated with larvae of the sea urchin Strongylocentrotus droebachiensis

Animals acclimate to changes in their environment through diverse responses, including phenotypic plasticity and shifts in their microbiome. These microbial communities are also taxonomically distinct across the geographical distribution of the host. It is less known, however, whether taxonomic differences in host-associated bacterial communities between geographically distinct populations mask shifts due to environmental changes within a population. We tested for potential ecological masking using larvae of the echinoid Strongylocentrotus droebachiensis from three coastal locations in the Pacific and Atlantic Oceans that were exposed to four feeding regimes. When considering OTU membership and the relative proportion of those taxa, the composition of the larval-associated bacterial communities were best explained by location, not feeding regime. Similarly, predicted metagenomic gene profiles from these bacterial communities were congruent with population specificity and may suggest a role in metabolism. We hypothesize that, while much of the differences in the bacterial communities is related to the large geographic distances between these locations, the predicted overlapping functions of the microbiome may relate to responding to ecological variation experienced by these larvae. Taken together, these results suggest that differences in community composition between populations masks local variation, and that scaling should be considered in when studying microbiome dynamics.

ecology↗

bioRxiv2018

Optimizing non-invasive sampling of an infectious bat virus

Notable outbreaks of infectious viruses resulting from spillover events from bats have brought much attention to the ecological origins of bat-borne zoonoses, resulting in an increase in ecological and epidemiological studies on bat populations in Africa, Asia, and Australia. The aim of many of these studies is to identify new viral agents with field sampling methods that collect pooled urine samples from large plastic sheets placed under a bat roost. The efficiency of under-roost sampling also makes it an attractive method for gathering roost-level prevalence data. However, the method allows multiple individuals to contribute to a pooled sample, potentially introducing positive bias. To assess the ability of under-roost sampling to accurately estimate viral prevalence, we constructed a probabilistic model to explore the relationship between four sampling designs (quadrant, uniform, stratified, and random) and estimation bias. We modeled bat density and movement with a Poisson cluster process and spatial kernels, and simulated the four underroost sheet sampling designs by manipulating a spatial grid of hexagonal tiles. We performed global sensitivity analyses to identify major sources of estimation bias and provide recommendations for field studies that wish to estimate roost-level prevalence. We found that the quadrant-based design had a positive bias 5-7 times higher than other designs due to spatial auto-correlation among sampling sheets and clustering of bats in the roost. The sampling technique is therefore highly sensitive to viral presence; but lacks specificity, providing poor information regarding dynamics in viral prevalence. Given population sizes of 5000-14000, our simulation results indicate that using a stratified random design to collect 30-40 urine samples from 80-100 sheets, each with an area of 0.75-1m2, would provide sufficient estimation of true prevalence with minimum sampling bias and false negatives. However, acknowledging the general problem of data aggregation, we emphasize that robust inference of true prevalence from field data require information of underpinning roost sizes. Our findings refine our understanding of the underroost sampling technique with the aim of increasing its specificity, and suggest that the method be further developed as an efficient non-invasive sampling technique that provides roost-level estimates of viral prevalence within a bat population.

ecology↗

bioRxiv2018

Genome-skimming provides accurate quantification for pollen mixtures

In the face of global pollinator declines, plant-pollinator interaction networks have been studied to guide ecological conservation and restoration. In order to obtain more comprehensive and unbiased knowledge of these networks, perspectives of both plants and pollinators need to be considered integratively. Metabarcoding has seen increasing applications in characterizing pollen transported by pollinators. However, amplification bias across taxa could lead to unpredictable artefacts in pollen compositions. We examined the efficacy of a PCR-free genome-skimming method in quantifying mixed pollen, using mock samples constructed with known pollen species (5 mocks of flower pollen and 14 mocks of bee pollen). The results demonstrated a high level of repeatability and accuracy in identifying pollen from mixtures of varied species ratios. All pollen species were detected in all mock samples, and pollen frequencies estimated from the number of sequence reads of each species were significantly correlated with pollen count proportions (linear model, R2 =86.7%, P = 2.2e- 16). For >97% of the mixed taxa, pollen proportion could be quantified by sequencing to the correct order of magnitude, even for species which constituted only 0.2% of the total pollen. We also showed that DNA extracted from pollen grains equivalent to those collected from a single honeybee corbicula was sufficient for the genome-skimming pipeline. We conclude that genome-skimming is a feasible approach to identifying and quantifying pollen compositions for mixed pollen samples. By providing reliable and sensitive taxon identification and relative abundance, this method is expected to improve the understanding of pollen diversity transported by pollinators and their ecological roles in the plant-pollinator networks.

ecology↗

bioRxiv2018

Monitoring the eradication of the highly invasive topmouth gudgeon (Pseudorasbora parva) using a novel eDNA assay

Aquatic Invasive Species (AIS) represent an important threat for Biodiversity and are one of the factors determining the ecological integrity of water bodies under the Water Framework Directive. Eradication is one of the most effective tools for the management of invasive species but has important economic and ecological trade-offs and its success needs to be carefully monitored. We assessed the eradication success of the topmouth gudgeon (Pseudorasbora parva), an invasive fish that poses significant risks to endemic aquatic fauna, in four ponds previously treated with the piscicide Rotenone using a novel environmental DNA (eDNA)-qPCR assay. Topmouth gudgeon was detected in all four treated ponds using 750 mL water samples and in three of the ponds using 15 mL samples, despite the eradication treatment. The highly sensitive qPCR assay detected topmouth gudgeon in a significantly greater proportion of sites (77.5%) than eDNA detection methods based on conventional PCR (35%). Our results highlight the difficulties of eradicating invasive fish and the need to incorporate reliable monitoring methods as part of a risk management strategy under the Water Framework Directive.

ecology↗

bioRxiv2018

Specific metabolic signatures of fish exposed to cyanobacterial blooms

With the increasing impact of the global warming, occurrences of cyanobacterial blooms in aquatic ecosystems are becoming a main ecological concern around the world. Due to their capacity to produce potential toxic metabolites, interactions between the cyanobacteria/cyanotoxin complex and the other freshwater organisms have been widely studied in the past years. Non-targeted metabolomic analyses have the powerful capacity to study a high number of metabolites at the same time and thus to understand in depth the molecular interactions between various organisms in different environmental scenario and notably during cyanobacterial blooms. In this way during summer 2015, liver metabolomes of two fish species, sampled in peri-urban lakes of the ile-de-France region containing or not high concentrations of cyanobacteria, were studied. The results suggest that similar metabolome changes occur in both fish species exposed to cyanobacterial blooms compared to them not exposed. Metabolites implicated in protein synthesis, protection against ROS, steroid metabolism, cell signaling, energy storage and membrane integrity/stability have shown the most contrasted changes. Furthermore, it seems that metabolomic studies will provide new information and research perspectives in various ecological fields and notably concerning cyanobacteria/fish interactions but also a promising tool for environmental monitoring of water pollutions.

ecology↗

bioRxiv2018

Network of small no-take marine reserves reveal greater abundance and body size of fisheries target species

No-take marine reserves (NTRs), i.e. areas with total fishing restrictions, have been established worldwide aiming to provide biodiversity and ecosystem conservation. Brazil has established NTRs, but currently lacks scientific knowledge and understanding of their ecological role, particularly regarding rocky reefs in subtropical regions. Consequently, this study aimed to contrast NTR, from the 30 year old Tupinambas Ecological Station, and comparable fished sites across a coastal biogeographic gradient to investigate the effect of fishing and habitat variability on the abundance and body-size of rocky reef fish. We used Baited Remote Underwater stereo-Video (stereo-BRUVs) and Diver Operated stereo-Video (stereo-DOVs) systems to simultaneously sample reef fish and habitat. Model selection and results identified habitat and biogeographic variables, such as distance from shore, as important predictor variables, explaining several aspects of the fish assemblage. The effect of protection was important in determining the abundance and body-size of targeted species, in particular for epinephelids and carangids. Conversely, species richness was correlated with habitat complexity and not with protection status. This is the first study to publish data using these novel survey methods in the Southeastern Atlantic and demonstrate their utility, in combination with an established network of NTRs, to provide benchmarks for conservation and fisheries management.

ecology↗

bioRxiv2018

A comparative study of ‘safe and just operating space’ for the south and south-east Asian countries

The world is presently maintaining a delicate balance of continuing well-being and social development for the people through consumption of biophysical resources of nature without topping global average per capita availability. In this paper, we have framed a per capita top-down framework to survey national safe and just operating space (NSJOS) for the countries of south and southeast Asia to understand past variations and as a consequence, the present scenario. Amalgamating 27 indicators, all regarding Sustainable Development Goals (except - SDG 17), in consort with their respective environmental boundaries or desirable social development thresholds, this study explores into both biophysical (for ecological stress) and social development (for social deprivation) attributes of 19 countries of south and southeast Asia. This analysis shows, only 2 have remained either unchanged (political voice) or declining (social equity) among the 12 dimensions of social development in countries of this region. The remaining 10 dimensions of social development showing positive progress and will meet corresponding desired thresholds of United Nations Sustainable Development Goals 2015. All the 7 indicators showing tendencies of overconsumption of biophysical resources, that might be leading to exceeding per capita global average planetary boundaries in forthcoming future. However, ecological boundaries have remained protected to a decent degree so far for these countries. The challenge would be to maintain and increase the pace of social development and bringing it in equal strata of a global standard in future without depleting drivers of these, i.e. biophysical resources. National policy adaptations are crucial if these countries of south and southeast Asia desire to bring about adequacy in biophysical resources reserve whilst granting social equity in access and exploitation of these resources for the people towards the persistant social development in impending decades.

ecology↗

bioRxiv2018

Macroscale estimates of species abundance reveal evolutionary drivers of biodiversity

Evolutionary processes underpin the biodiversity on the planet. Theories advocate that the form of the species abundance distribution (SAD), presented by the number of individuals for each species within an ecological community, is intimately linked to speciation modes such as point mutation and random fission. This prediction has rarely been, however, verified empirically; the fact that species abundance data can be obtained only from local communities critically limits our ability to infer the role of macroevolution in shaping ecological patterns. Here, we developed a novel statistical model to estimate macroscale SADs, the hidden macroecological property, by integrating spatially replicated multispecies detection-nondetection observations and the data on species geographic distributions. We determined abundance of 1,248 woody plant species at a 10 km grid square resolution over East Asian islands across subtropical to temperate biomes, which produced a metacommunity (i.e. species pool) SAD in four insular ecoregions along with its absolute size. The metacommunity SADs indicated lognormal-like distributions, which were well explained by the unified neutral theory of biodiversity and biogeography (UNTB) with protracted speciation, a mode of speciation intermediate between point mutation and random fission. Furthermore, the analyses yielded an estimate of speciation rate in each region that highlighted the importance of geographic characteristics in macroevolutionary processes and predicted the average species lifetime that was congruent with previous estimates. The estimation of macroscale SADs plays a remarkable role in revealing evolutionary diversification of regional species pools.

ecology↗

bioRxiv2018

Male and female bees show large differences in floral preference

O_LIIntraspecific variation in foraging niche can drive food web dynamics and ecosystem processes. Field studies and theoretical analysis of plant-pollinator interaction networks typically focus on the partitioning of the floral community between pollinator species, with little attention paid to intraspecific variation among plants or foraging bees. In other systems, male and female animals exhibit different, cascading, impacts on interaction partners. Although the foraging ecology of male bees is little known, we expect foraging preferences to differ between male and female bees, which could strongly impact plant-pollinator interaction outcomes.\nC_LIO_LIWe designed an observational study to evaluate the strength and prevalence of sexually dimorphic foraging preferences in bees.\nC_LIO_LIWe observed bees visiting flowers in semi-natural meadows in New Jersey, USA. To detect differences in flower use against a shared background resource availability, we maximized the number of interactions observed within narrow spatio-temporal windows. To distinguish observed differences in bee use of flower species, which can reflect abundance patterns and sampling effects, from underlying differences in bee preferences, we analyzed our data with both a permutation-based null model and random effects models.\nC_LIO_LIWe found that the diets of male and female bees of the same species were often as dissimilar as the diets of bees of different species. Furthermore, we demonstrate differences in preference between male and female bees, and identify plant species that are particularly attractive to each sex. We show that intraspecific differences in preference can be robustly identified within interactions between hundreds of species, without precisely quantifying resource availability, and despite high phenological turnover.\nC_LIO_LIGiven the large differences in flower use and preference between male and female bees, ecological sex differences should be integrated into studies of bee demography, plant pollination, and coevolutionary relationships between flowers and insects.\nC_LI

ecology↗

bioRxiv2018

A 117 year retrospective analysis of Pennsylvania tick community dynamics

BackgroundTick-borne diseases have been increasing at the local, national, and global levels. Researchers studying ticks and tick-borne disease need a thorough knowledge of the pathogens, vectors, and epidemiology of disease spread. Three surveillance approaches are commonly used to provide insight into tick-borne disease risk: human disease case surveillance, active tick surveillance, and passive tick surveillance. Long-term passive surveillance can provide up-to-date data on the spatial variability and temporal dynamics of ectoparasite communities and shed light into the ecology of rarer tick species. We present a retrospective analysis on compiled data of ticks from Pennsylvania over the last 117 years.\n\nMethodsWe compiled data from ticks collected during tick surveillance research, and from citizen-based submissions to the Penn State University Department of Entomology (PSUEnt). Specimens were deposited at the PSUEnt arthropod collections that eventually became The Frost Entomological Museum. While most of the specimens were submitted by the public, a subset of the data were collected through active methods (flagging or dragging, or removal of ticks from wildlife). We analyzed all data from 1900-2017 for tick community composition, host associations, and spatio-temporal dynamics.\n\nResultsIn total there were 4,491 submission lots consisting of 7,132 tick specimens. Twenty-four different species were identified, with the large proportion of submissions represented by five tick species. We observed a shift in tick community composition in which the dominant species of tick (Ixodes cookei) was overtaken in abundance by Dermacentor variabilis in the early 1990s, and then replaced in abundance by I. scapularis. We analyzed host data and identified overlaps in host range amongst tick species, suggesting potential hubs of pathogen transfer between different tick vectors and their reservoir hosts.\n\nConclusionsWe highlight the importance of long-term passive tick surveillance in investigating the ecology of both common and rare tick species. Information on the geographic distribution, host-association, and seasonality of the tick community can help researchers and health-officials to identify high-risk areas.

ecology↗

bioRxiv2018

Anthropogenic remediation of heavy metals selects against natural microbial remediation

In an era of unprecedented environmental change, there have been increasing ecological and global public health concerns associated with exposure to anthropogenic pollutants. While there is a pressing need to remediate polluted ecosystems, human intervention strategies might unwittingly oppose selection for natural detoxification, which is primarily carried out by microbes. We test this possibility in the context of a ubiquitous chemical remediation strategy aimed at targeting toxic metal pollution: the addition of lime-containing materials. Here we show that raising pH by liming decreased the availability of toxic metals in acidic mine-degraded soils, but as a consequence selected against microbial taxa that naturally remediate soil through the production of metal-scavenging siderophores. Understanding the ecological and evolutionary consequences of human intervention on key traits is crucial for the engineering of evolutionary resilient microbial communities, having important implications for human health and biotechnology.

ecology↗

bioRxiv2018

Ecosystem tipping points in an evolving world

There is growing concern over tipping points arising in ecosystems due to the crossing of environmental thresholds. Tipping points lead to strong and possibly irreversible shifts between alternative ecosystem states incurring high societal costs. Traits are central to the feedbacks that maintain alternative ecosystem states, as they govern the responses of populations to environmental change that could stabilize or destabilize ecosystem states. However, we know little about how evolutionary changes in trait distributions over time affect the occurrence of tipping points, and even less about how big scale ecological shifts reciprocally interact with trait dynamics. We argue that interactions between ecological and evolutionary processes should be taken into account for understanding the balance of feedbacks governing tipping points in nature.

ecology↗

bioRxiv2018

Effect of fire and thinning on fine-scale genetic structure and gene flow in fire-suppressed populations of sugar pine (Pinus lambertiana Douglas)

Historically, frequent, low-severity fires in dry western North American forests were a major driver of ecological patterns and processes, creating resilient ecosystems dominated by widely-spaced pine species. However, a century of fire-suppression has caused overcrowding, altering forest composition to shade-tolerant species, while increasing competition and leaving trees stressed and susceptible to pathogens, insects, and high-severity fire. Exacerbating the issue, fire incidence is expected to increase with changing climate, while fire season has been observed to begin earlier and last longer than historic trends. Forest thinning and prescribed fire have been identified as important management tools to mitigate these risks. Yet little is known of how thinning, fire, or their interaction affect contemporary evolutionary processes of constituent pine species that influence fitness and play an important role in the opportunity for selection and population persistence. We assessed the impact of widely used fuel reduction treatments and prescribed fire on fine-scale gene flow on an ecologically important and historically dominant shade-intolerant pine species of the Sierra Nevada, Pinus lambertiana Dougl. Treatment prescription (no-thin-no-fire, thin-no-fire, and fire-and-thin) was found to differentially affect both fine-scale spatial and genetic structure as well as effective gene flow in this species. Specifically, the thin-no-fire prescription increases genetic structure (spatial autocorrelation of relatives) between adults and seedlings, while seed and pollen dispersal increase and decrease, respectively, as a function of increasing disturbance intensity. While these results may be specific to the stands at our study site, they indicate how assumptions relating to genetic effects based on spatial structure can be misleading. It is likely that these disequilibrated systems will continue to evolve on unknown evolutionary trajectories. The long-term impacts of management practices on reduced fitness from inbreeding depression should be continually monitored to ensure resilience to increasingly frequent and severe fire, drought, and pest stresses.

ecology↗

bioRxiv2018

Taking a deeper look: Quantifying the differences in fish assemblages between shallow and mesophotic temperate rocky reefs

The spatial distribution of a species assemblage is often determined by habitat and climate. In the marine environment, depth can become an important factor as degrading light leads to changes in the biological habitat structure. To date, much of the focus of ecological fish research has been based on reefs in less than 40 m with little research on the ecological role of mesophotic reefs. We deployed baited remote underwater stereo video systems (stereo-BRUVS) on temperate reefs in two depth categories: shallow (20-40m) and mesophotic (80-120m), off Port Stephens, Australia. Sites were selected using data collected by swath acoustic sounder to ensure stereo-BRUVS were deployed on reef. The sounder also provided rugosity, slope and relief data for each stereo-BRUVS deployment. Multivariate analysis indicates that there are significant differences in the fish assemblages between shallow and mesophotic reefs, primarily driven by Ophthalmolepis lineolatus and Notolabrus gymnogenis only occurring on shallow reefs and schooling species of fish that were unique to each depth category: Atypichthys strigatus on shallow reefs and Centroberyx affinis on mesophotic reefs. While shallow reefs had a greater species richness and abundance of fish when compared to mesophotic reefs, mesophotic reefs hosted the same species richness of fishery targeted species. Chrysophrys auratus (pink snapper) and Nemodactylus douglassii (grey morwong) are two highly targeted species in this region. While C. auratus was numerically more abundant on shallow reefs, mesophotic reefs provide habitat for larger fish. In comparison, N. douglassii were evenly distributed across all sites sampled. Generalized linear models revealed that depth and habitat type provided the most parsimonious model for predicting the distribution of C. auratus, while habitat type alone best predicted the distribution of N. douglassii. These results demonstrate the importance of mesophotic reefs to fishery targeted species and therefore have implications for informing the management of these fishery resources on shelf rocky reefs.

ecology↗

bioRxiv2018

Insights on the assembly rules of a continent-wide multilayer network

Introductory paragraphHow are ecological systems assembled? Here, we aim to contribute to answering this question by harnessing the framework of a novel integrative hypothesis. We shed light on the assembly rules of a multilayer network formed by frugivory and nectarivory interactions between bats and plants in the Neotropics. Our results suggest that, at a large scale, phylogenetic trade-offs separate species into different layers and modules. At an intermediate scale, the modules are also shaped by geographic trade-offs. And at a small scale, the network shifts to a nested structure within its modules, probably as a consequence of resource breadth processes. Finally, once the topology of the network is shaped, morphological traits related to consuming fruits or nectar determine which species are central or peripheral. Our results help understand how different processes contribute to the assemblage of ecological systems at different scales, resulting in a compound topology.

ecology↗

bioRxiv2026

From concentration to export: resource contrasts and bee traits shape pollinator spillover to crops

Floral plantings can either concentrate bees or export them to adjacent crops, yet the ecological conditions influencing these outcomes remain unclear. Here, we develop a mathematical model as proof of concept for our previous integrative hypothesis: concentrator and exporter outcomes can arise as alternative, context-dependent outcomes of the same underlying resource-selection process. Using bees as a model and focusing specifically on spillover from floral plantings to crops, we identified resource-specific thresholds separating concentration- and export-favoring conditions. Our model translates differences in relative patch attractiveness into context-dependent concentration and export outcomes and generates resource-specific, testable predictions about the conditions favoring pollinator movement into crops. In our simulations, the concentrator-exporter transition occurred at a lower flowering-intensity contrast than at pollen or nectar contrasts, which suggests that flowering intensity may provide an initial cue for bee movement, whereas nectar and pollen rewards refine or sustain bee responses once crops are perceived as attractive. Spillover thresholds differed among resource contrasts, whereas response steepness varied across bee-trait and community scenarios. Under the model's trait-sensitivity formulation, predicted spillover probability responded more strongly to flowering contrast for specialists than for generalists; colony size amplified this response, whereas bee richness dampened it. Together, these patterns show how flowering and resource contrasts interact with bee traits and community context to shape predicted spillover. Our results confirm that the concentrator and exporter hypotheses can be understood as context-dependent outcomes of the same ecological process rather than as mutually exclusive alternatives. Experimental tests of the predicted thresholds conducted in the field could reveal when and where floral plantings are most likely to promote bee spillover to crops, potentially supporting crop pollination.

ecology↗

bioRxiv2013

Speciation and introgression between Mimulus nasutus and Mimulus guttatus

Mimulus guttatus and M. nasutus are an evolutionary and ecological model sister species pair differentiated by ecology, mating system, and partial reproductive isolation. Despite extensive research on this system, the history of divergence and differentiation in this sister pair is unclear. We present and analyze a novel population genomic data set which shows that M. nasutus "budded" off of a central Californian M. guttatus population within the last 200 to 500 thousand years. In this time, the M. nasutus genome has accrued numerous genomic signatures of the transition to predominant selfing. Despite clear biological differentiation, we document ongoing, bidirectional introgression. We observe a negative relationship between the recombination rate and divergence between M. nasutus and sympatric M. guttatus samples, suggesting that selection acts against M. nasutus ancestry in M. guttatus.

Evolutionary Biology↗