Boom-bust population dynamics drive rapid genetic change.

Increasing environmental threats and more extreme environmental perturbations place species at risk of population declines, with associated loss of genetic diversity and evolutionary potential. While theory shows that rapid population declines can cause loss of genetic diversity, populations in some environments, like Australia's arid zone, are repeatedly subject to major population fluctuations yet persist and appear able to maintain genetic diversity. Here, we use repeated population sampling over 13 y and genotype-by-sequencing of 1903 individuals to investigate the genetic consequences of repeated population fluctuations in two small mammals in the Australian arid zone. The sandy inland mouse (Pseudomys hermannsburgensis) experiences marked boom-bust population dynamics in response to the highly variable desert environment. We show that heterozygosity levels declined, and population differentiation (FST) increased, during bust periods when populations became small and isolated, but that heterozygosity was rapidly restored during episodic population booms. In contrast, the lesser hairy-footed dunnart (Sminthopsis youngsoni), a desert marsupial that maintains relatively stable population sizes, showed no linear declines in heterozygosity. These results reveal two contrasting ways in which genetic diversity is maintained in highly variable environments. In one species, diversity is conserved through the maintenance of stable population sizes across time. In the other species, diversity is conserved through rapid genetic mixing during population booms that restores heterozygosity lost during population busts.

slimr: An R package for tailor-made integrations of data in population genomic simulations over space and time.

Software for realistically simulating complex population genomic processes is revolutionizing our understanding of evolutionary processes, and providing novel opportunities for integrating empirical data with simulations. However, the integration between standalone simulation software and R is currently not well developed. Here, we present slimr, an R package designed to create a seamless link between standalone software SLiM >3.0, one of the most powerful population genomic simulation frameworks, and the R development environment, with its powerful data manipulation and analysis tools. We show how slimr facilitates smooth integration between genetic data, ecological data and simulation in a single environment. The package enables pipelines that begin with data reading, cleaning and manipulation, proceed to constructing empirically based parameters and initial conditions for simulations, then to running numerical simulations and finally to retrieving simulation results in a format suitable for comparisons with empirical data - aided by advanced analysis and visualization tools provided by R. We demonstrate the use of slimr with an example from our own work on the landscape population genomics of desert mammals, highlighting the advantage of having a single integrated tool for both data analysis and simulation. slimr makes the powerful simulation ability of SLiM directly accessible to R users, allowing integrated simulation projects that incorporate empirical data without the need to switch between software environments. This should provide more opportunities for evolutionary biologists and ecologists to use realistic simulations to better understand the interplay between ecological and evolutionary processes.

Episodic population fragmentation and gene flow reveal a trade-off between heterozygosity and allelic richness.

In episodic environments like deserts, populations of some animal species exhibit irregular fluctuations such that populations are alternately large and connected or small and isolated. Such dynamics are typically driven by periodic resource pulses due, for example, to large but infrequent rainfall events. The repeated population bottlenecks resulting from fragmentation should lower genetic diversity over time, yet species undergoing these fluctuations appear to maintain high levels of genetic diversity. To resolve this apparent paradox, we simulated a metapopulation of constant size undergoing repeat episodes of fragmentation and change in gene flow to mimic outcomes experienced by mammals in an Australian desert. We show that episodic fragmentation and gene flow have contrasting effects on two measures of genetic diversity: heterozygosity and allelic richness. Specifically, fragmentation into many, small subpopulations, coupled with periods of infrequent gene flow, preserves allelic richness at the expense of heterozygosity. In contrast, fragmentation into a few, large subpopulations maintains heterozygosity at the expense of allelic richness. The strength of the trade-off between heterozygosity and allelic richness depends on the amount of gene flow and the frequency of gene flow events. Our results imply that the type of genetic diversity maintained among species living in strongly fluctuating environments will depend on the way populations fragment, with our results highlighting different mechanisms for maintaining allelic richness and heterozygosity in small, fragmented populations.

An invasive pathogen drives directional niche contractions in amphibians.

Global change is causing an unprecedented restructuring of ecosystems, with the spread of invasive species being a key driver. While population declines of native species due to invasives are well documented, much less is known about whether new biotic interactions reshape niches of native species. Here we quantify geographic range and realized-niche contractions in Australian frog species following the introduction of amphibian chytrid fungus Batrachochytrium dendrobatidis, a pathogen responsible for catastrophic amphibian declines worldwide. We show that chytrid-impacted species experienced proportionately greater contractions in niche breadth than geographic distribution following chytrid emergence. Furthermore, niche contractions were directional, with contemporary distributions of chytrid-impacted species characterized by higher temperatures, lower diurnal temperature range, higher precipitation and lower elevations. Areas with these conditions may enable host persistence with chytrid through lower pathogenicity of the fungus and/or greater demographic resilience. Nevertheless, contraction to a narrower subset of environmental conditions could increase host vulnerability to other threatening processes and should be considered in assessments of extinction risk and during conservation planning. More broadly, our results emphasize that biotic interactions can strongly shape species realized niches and that large-scale niche contractions due to new species interactions-particularly emerging pathogens-could be widespread.

Effects of harvesting and stubble management on abundance of pest rodents (Mus musculus) in a conservation agriculture system.

BACKGROUND: The shift to more environmentally sensitive agricultural practices over the last several decades has changed farmland landscapes worldwide. Changes including no-till and retaining high biomass mulch has been coincident with an increase in rodent pests in South Africa, India, South America and Europe, indicating a possible conflict between conservation agriculture (CA) and rodent pest management. Research on effects of various crop management practices associated with CA on pest rodent population dynamics is needed to anticipate and develop CA-relevant management strategies. RESULTS: During the Australian 2020-2021 mouse plague, farmers used postharvest stubble management practices, including flattening and/or cutting, to reduce stubble cover in paddocks to lessen habitat suitability for pest house mice. We used this opportunity to assess the effects of both harvest and stubble management on the movement and abundance of mice in paddocks using mouse trapping and radio tracking. We found that most tracked mice remained resident in paddocks throughout harvest, and that mouse population abundance was generally unaffected by stubble management. CONCLUSION: Recent conversions to CA practices have changed how pest house mice use cropped land. Management practices that reduce postharvest habitat complexity do not appear to reduce the attractiveness of paddocks to mice, and further research into new management strategies in addition to toxic bait use is required as part of an integrated pest management approach. © 2023 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Climate warming drives a temperate-zone lizard to its upper thermal limits, restricting activity, and increasing energetic costs.

Lizards are considered vulnerable to climate change because many operate near their thermal maxima. Exposure to higher temperatures could reduce activity of these animals by forcing them to shelter in thermal refugia for prolonged periods to avoid exceeding lethal limits. While rising temperatures should reduce activity in tropical species, the situation is less clear for temperate-zone species where activity can be constrained by both low and high temperatures. Here, we measure the effects of natural variation in environmental temperatures on activity in a temperate grassland lizard and show that it is operating near its upper thermal limit in summer even when sheltering in thermal refuges. As air temperatures increased above 32 °C, lizard activity declined markedly as individuals sought refuge in cool microhabitats while still incurring substantial metabolic costs. We estimate that warming over the last two decades has required these lizards to increase their energy intake up to 40% to offset metabolic losses caused by rising temperatures. Our results show that recent increases in temperature are sufficient to exceed the thermal and metabolic limits of temperate-zone grassland lizards. Extended periods of high temperatures could place natural populations of ectotherms under significantly increased environmental stress and contribute to population declines and extinction.

The cumulative impacts of anthropogenic stressors vary markedly along environmental gradients.

Understanding the cumulative effects of multiple stressors on biodiversity is key to managing their impacts. Stressor interactions are often studied using an additive/antagonistic/synergistic typology, aimed at identifying situations where individual stressor effects are reduced or amplified when they act in combination. Here, we analysed variation in the family richness of stream macroinvertebrates in the groups Ephemeroptera, Plecoptera and Trichoptera (EPT) at 4658 sites spanning a 32° latitudinal range in eastern Australia in relation to two largely human-induced stressors, salinity and turbidity, and two environmental gradients, temperature and slope. The cumulative and interactive effect of salinity and turbidity on EPT family richness varied across the landscape and by habitat (edge or riffle) such that we observed additive, antagonistic and synergistic outcomes depending on the environmental context. Our findings highlight the importance of understanding the consistency of multiple stressor impacts, which will involve higher-order interactions between multiple stressors and environmental factors.

Addressing context dependence in ecology.

Context dependence is widely invoked to explain disparate results in ecology. It arises when the magnitude or sign of a relationship varies due to the conditions under which it is observed. Such variation, especially when unexplained, can lead to spurious or seemingly contradictory conclusions, which can limit understanding and our ability to transfer findings across studies, space, and time. Using examples from biological invasions, we identify two types of context dependence resulting from four sources: mechanistic context dependence arises from interaction effects; and apparent context dependence can arise from the presence of confounding factors, problems of statistical inference, and methodological differences among studies. Addressing context dependence is a critical challenge in ecology, essential for increased understanding and prediction.

Phenotypic plasticity masks range-wide genetic differentiation for vegetative but not reproductive traits in a short-lived plant.

Genetic differentiation and phenotypic plasticity jointly shape intraspecific trait variation, but their roles differ among traits. In short-lived plants, reproductive traits may be more genetically determined due to their impact on fitness, whereas vegetative traits may show higher plasticity to buffer short-term perturbations. Combining a multi-treatment greenhouse experiment with observational field data throughout the range of a widespread short-lived herb, Plantago lanceolata, we (1) disentangled genetic and plastic responses of functional traits to a set of environmental drivers and (2) assessed how genetic differentiation and plasticity shape observational trait-environment relationships. Reproductive traits showed distinct genetic differentiation that largely determined observational patterns, but only when correcting traits for differences in biomass. Vegetative traits showed higher plasticity and opposite genetic and plastic responses, masking the genetic component underlying field-observed trait variation. Our study suggests that genetic differentiation may be inferred from observational data only for the traits most closely related to fitness.

Time lags and the invasion debt in plant naturalisations.

Ecological processes often exhibit time lags. For plant invasions, lags of decades to centuries between species' introduction and establishment in the wild (naturalisation) are common, leading to the idea of an invasion debt: accelerating rates of introduction result in an expanding pool of introduced species that will naturalise in the future. Here, I show how a concept from survival analysis, the hazard function, provides an intuitive way to understand and forecast time lags. For plant naturalisation, theoretical arguments predict that lags between introduction and naturalisation will have a unimodal distribution, and that increasing horticultural activity will cause the mean and variance of lag times to decline over time. These predictions were supported by data on introduction and naturalisation dates for plant species introduced to Britain. While increasing trade and horticultural activity can generate an invasion debt by accelerating introductions, the same processes could lower that debt by reducing lag times.

Globally, plant-soil feedbacks are weak predictors of plant abundance.

Plant-soil feedbacks (PSFs) have been shown to strongly affect plant performance under controlled conditions, and PSFs are thought to have far reaching consequences for plant population dynamics and the structuring of plant communities. However, thus far the relationship between PSF and plant species abundance in the field is not consistent. Here, we synthesize PSF experiments from tropical forests to semiarid grasslands, and test for a positive relationship between plant abundance in the field and PSFs estimated from controlled bioassays. We meta-analyzed results from 22 PSF experiments and found an overall positive correlation (0.12 ≤  r ¯  ≤ 0.32) between plant abundance in the field and PSFs across plant functional types (herbaceous and woody plants) but also variation by plant functional type. Thus, our analysis provides quantitative support that plant abundance has a general albeit weak positive relationship with PSFs across ecosystems. Overall, our results suggest that harmful soil biota tend to accumulate around and disproportionately impact species that are rare. However, data for the herbaceous species, which are most common in the literature, had no significant abundance-PSFs relationship. Therefore, we conclude that further work is needed within and across biomes, succession stages and plant types, both under controlled and field conditions, while separating PSF effects from other drivers (e.g., herbivory, competition, disturbance) of plant abundance to tease apart the role of soil biota in causing patterns of plant rarity versus commonness.

Reproductive ecology of a critically endangered alpine galaxiid.

Stocky galaxias Galaxias tantangara is a newly described freshwater fish restricted to a single population, occupying a 3 km reach of a small headwater stream in the upper Murrumbidgee River catchment of south-eastern Australia. This species is listed as critically endangered under IUCN Red List criteria, and knowledge of the species' ecology is critical for future conservation efforts to establish additional populations by translocation and captive breeding. This study details the first account of spawning and reproductive ecology of G. tantangara, including reproductive development, timing of spawning and a description of one spawning site. Peak gonadosomatic index was observed in March/April in males and in October in females. Absolute fecundity ranged from 211 oocytes for a 76 mm length to caudal fork (LCF) fish to 810 oocytes for a 100 mm LCF fish. The observation of spent females in mid-November 2017 and discovery of an egg mass 8 days later suggest that spawning had occurred, and over a relatively short period. Larvae were subsequently detected in monthly electrofishing surveys in December 2017. Findings from this study provide new understanding of existing and future threats to G. tantangara and have important implications for conservation management of not only this species but also other closely related threatened Galaxias species.

Eruptive dynamics are common in managed mammal populations.

Successful conservation management is often based on the principle that small or declining populations can recover if we identify and remove the factors that caused them to decline in the first place. But what form will that recovery take? Theory tells us that when a strong limiting factor is removed, a population should increase in size to where it becomes limited by some other factor. However, if the subsequent limitation involves feedbacks between the density of a consumer and its resource, there is potential for the consumer population to undergo substantial fluctuations in size that we would characterize as boom-bust or eruptive dynamics. We analysed long-term (7.6-29 yr) data documenting changes in the abundance of 169 populations of 20 mammal species released from a strong limiting factor (fox predation) in Australia. We show that many populations (44) exhibited eruptive dynamics, with exponential increase to a peak and subsequent population decline. Of 51 populations showing eruptive dynamics (the Australian populations plus seven translocated ungulate populations), the time taken for erupting populations to reach a peak before declining was related negatively to the intrinsic rate of population growth and positively to body mass, such that larger-bodied species with slow rates of population growth had a longer period of population increase before declining. Our results suggest that a substantial proportion of populations recovering after removal of a threatening process are likely to exhibit eruptive dynamics, and that managers of recovering or translocated populations should anticipate this outcome in conservation planning.

Phylogenetic signals and predictability in plant-soil feedbacks.

There is strong evidence for a phylogenetic signal in the degree to which species share co-evolved biotic partners and in the outcomes of biotic interactions. This implies there should be a phylogenetic signal in the outcome of feedbacks between plants and the soil microbiota they cultivate. However, attempts to identify a phylogenetic signal in plant-soil feedbacks have produced mixed results. Here we clarify how phylogenetic signals could arise in plant-soil feedbacks and use a recent compilation of data from feedback experiments to identify: whether there is a phylogenetic signal in the outcome of plant-soil feedbacks; and whether any signal arises through directional or divergent changes in feedback outcomes with evolutionary time. We find strong evidence for a divergent phylogenetic signal in feedback outcomes. Distantly related plant species show more divergent responses to each other's soil microbiota compared with closely related plant species. The pattern of divergence implies occasional co-evolutionary shifts in how plants interact with soil microbiota, with strongly contrasting feedback responses among some plant lineages. Our results highlight that it is difficult to predict feedback outcomes from phylogeny alone, other than to say that more closely related species tend to have more similar responses.

Identifying error and accurately interpreting environmental DNA metabarcoding results: A case study to detect vertebrates at arid zone waterholes.

Environmental DNA (eDNA) metabarcoding surveys enable rapid, noninvasive identification of taxa from trace samples with wide-ranging applications from characterizing local biodiversity to identifying food-web interactions. However, the technique is prone to error from two major sources: (a) contamination through foreign DNA entering the workflow, and (b) misidentification of DNA within the workflow. Both types of error have the potential to obscure true taxon presence or to increase taxonomic richness by incorrectly identifying taxa as present at sample sites, but multiple error sources can remain unaccounted for in metabarcoding studies. Here, we use data from an eDNA metabarcoding study designed to detect vertebrate species at waterholes in Australia's arid zone to illustrate where and how in the workflow errors can arise, and how to mitigate those errors. We detected the DNA of 36 taxa spanning 34 families, 19 orders and five vertebrate classes in water samples from waterholes, demonstrating the potential for eDNA metabarcoding surveys to provide rapid, noninvasive detection in remote locations, and to widely sample taxonomic diversity from aquatic through to terrestrial taxa. However, we initially identified 152 taxa in the samples, meaning there were many false positive detections. We identified the sources of these errors, allowing us to design a stepwise process to detect and remove error, and provide a template to minimize similar errors that are likely to arise in other metabarcoding studies. Our findings suggest eDNA metabarcoding surveys need to be carefully conducted and screened for errors to ensure their accuracy.

The relationship between propagule pressure and establishment success in alien bird populations: a re-analysis of Moulton & Cropper (2019).

A recent analysis by Moulton & Cropper (2019) of a global dataset on alien bird population introductions claims to find no evidence that establishment success is a function of the size of the founding population. Here, we re-analyse Moulton & Cropper's data and show that this conclusion is based on flawed statistical methods-their data in fact confirm a strong positive relationship between founding population size and establishment success. We also refute several non-statistical arguments against the likelihood of such an effect presented by Moulton & Cropper. We conclude that a core tenet of population biology-that small populations are more prone to extinction-applies to alien populations beyond their native geographic range limits as much as to native populations within them.

Global gene flow releases invasive plants from environmental constraints on genetic diversity.

When plants establish outside their native range, their ability to adapt to the new environment is influenced by both demography and dispersal. However, the relative importance of these two factors is poorly understood. To quantify the influence of demography and dispersal on patterns of genetic diversity underlying adaptation, we used data from a globally distributed demographic research network comprising 35 native and 18 nonnative populations of Plantago lanceolata Species-specific simulation experiments showed that dispersal would dilute demographic influences on genetic diversity at local scales. Populations in the native European range had strong spatial genetic structure associated with geographic distance and precipitation seasonality. In contrast, nonnative populations had weaker spatial genetic structure that was not associated with environmental gradients but with higher within-population genetic diversity. Our findings show that dispersal caused by repeated, long-distance, human-mediated introductions has allowed invasive plant populations to overcome environmental constraints on genetic diversity, even without strong demographic changes. The impact of invasive plants may, therefore, increase with repeated introductions, highlighting the need to constrain future introductions of species even if they already exist in an area.

Application of DArT seq derived SNP tags for comparative genome analysis in fishes; An alternative pipeline using sequence data from a non-traditional model species, Macquaria ambigua.

Bi-allelic Single Nucleotide Polymorphism (SNP) markers are widely used in population genetic studies. In most studies, sequences either side of the SNPs remain unused, although these sequences contain information beyond that used in population genetic studies. In this study, we show how these sequence tags either side of a single nucleotide polymorphism can be used for comparative genome analysis. We used DArTseq (Diversity Array Technology) derived SNP data for a non-model Australian native freshwater fish, Macquaria ambigua, to identify genes linked to SNP associated sequence tags, and to discover homologies with evolutionarily conserved genes and genomic regions. We concatenated 6,776 SNP sequence tags to create a hypothetical genome (representing 0.1-0.3% of the actual genome), which we used to find sequence homologies with 12 model fish species using the Ensembl genome browser with stringent filtering parameters. We identified sequence homologies for 17 evolutionarily conserved genes (cd9b, plk2b, rhot1b, sh3pxd2aa, si:ch211-148f13.1, si:dkey-166d12.2, zgc:66447, atp8a2, clvs2, lyst, mkln1, mnd1, piga, pik3ca, plagl2, rnf6, sec63) along with an ancestral evolutionarily conserved syntenic block (euteleostomi Block_210). Our analysis also revealed repetitive sequences covering approximately 12% of the hypothetical genome where DNA transposon, LTR and non-LTR retrotransposons were most abundant. A hierarchical pattern of the number of sequence homologies with phylogenetically close species validated the approach for repeatability. This new approach of using SNP associated sequence tags for comparative genome analysis may provide insight into the genome evolution of non-model species where whole genome sequences are unavailable.

Karyotypes and Sex Chromosomes in Two Australian Native Freshwater Fishes, Golden Perch (Macquaria ambigua) and Murray Cod (Maccullochella peelii) (Percichthyidae).

Karyotypic data from Australian native freshwater fishes are scarce, having been described from relatively few species. Golden perch (Macquaria ambigua) and Murray cod (Maccullochella peelii) are two large-bodied freshwater fish species native to Australia with significant indigenous, cultural, recreational and commercial value. The arid landscape over much of these fishes' range, coupled with the boom and bust hydrology of their habitat, means that these species have potential to provide useful evolutionary insights, such as karyotypes and sex chromosome evolution in vertebrates. Here we applied standard and molecular cytogenetic techniques to characterise karyotypes for golden perch and Murray cod. Both species have a diploid chromosome number 2n = 48 and a male heterogametic sex chromosome system (XX/XY). While the karyotype of golden perch is composed exclusively of acrocentric chromosomes, the karyotype of Murray cod consists of two submetacentric and 46 subtelocentric/acrocentric chromosomes. We have identified variable accumulation of repetitive sequences (AAT)10 and (CGG)10 along with diverse methylation patterns, especially on the sex chromosomes in both species. Our study provides a baseline for future cytogenetic analyses of other Australian freshwater fishes, especially species from the family Percichthyidae, to better understand their genome and sex chromosome evolution.

Resolving the invasion paradox: pervasive scale and study dependence in the native-alien species richness relationship.

The degree to which plant communities are vulnerable to invasion by alien species has often been assessed using the relationship between native and alien plant species richness (NAR). Variation in the direction and strength of the NAR tends to be negative for small plot sizes and study extents, but positive for large plots and extents. This invasion paradox has been attributed to different processes driving species richness at different spatial scales. However, the focus on plot size has drawn attention away from other factors influencing the NAR, in part because the influence of other factors may be obscured by or interact with plot size. Here, we test whether variation in the NAR can be explained by covariates linked to community susceptibility to invasion and whether these interact with plot size using a quantitative meta-analysis drawn from 87 field studies that examined 161 NARs. While plot size explained most variation, the NAR was less positive in grassland habitats and in the Australasian region. Other covariates did not show strong relationships with the NAR even after accounting for interactions with plot size. Instead, much of the unexplained variation is associated with article or author specific differences, suggesting the NAR depends strongly on how different authors choose their study system or study design.