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.

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.

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.

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.

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.

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.

Import volumes and biosecurity interventions shape the arrival rate of fungal pathogens.

Global trade and the movement of people accelerate biological invasions by spreading species worldwide. Biosecurity measures seek to allow trade and passenger movements while preventing incursions that could lead to the establishment of unwanted pests, pathogens, and weeds. However, few data exist to evaluate whether changes in trade volumes, passenger arrivals, and biosecurity measures have altered rates of establishment of nonnative species over time. This is particularly true for pathogens, which pose significant risks to animal and plant health and are consequently a major focus of biosecurity efforts but are difficult to detect. Here, we use a database of all known plant pathogen associations recorded in New Zealand to estimate the rate at which new fungal pathogens arrived and established on 131 economically important plant species over the last 133 years. We show that the annual arrival rate of new fungal pathogens increased from 1880 to about 1980 in parallel with increasing import trade volume but subsequently stabilised despite continued rapid growth in import trade and recent rapid increases in international passenger arrivals. Nevertheless, while pathogen arrival rates for crop and pasture species have declined in recent decades, arrival rates have increased for forestry and fruit tree species. These contrasting trends between production sectors reflect differences in biosecurity effort and suggest that targeted biosecurity can slow pathogen arrival and establishment despite increasing trade and international movement of people.

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.

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.

Seed dispersal increases local species richness and reduces spatial turnover of tropical tree seedlings.

Dispersal is thought to be a key process underlying the high spatial diversity of tropical forests. Just how important dispersal is in structuring plant communities is nevertheless an open question because it is very difficult to isolate dispersal from other processes, and thereby measure its effect. Using a unique situation, the loss of vertebrate seed dispersers on the island of Guam and their presence on the neighboring islands of Saipan and Rota, we quantify the contribution of vertebrate seed dispersal to spatial patterns of diversity of tree seedlings in treefall gaps. The presence of vertebrate seed dispersers approximately doubled seedling species richness within canopy gaps and halved species turnover among gaps. Our study demonstrates that dispersal plays a key role in maintaining local and regional patterns of diversity, and highlights the potential for ongoing declines in vertebrate seed dispersers to profoundly alter tropical forest composition.

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.

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.

Does Size Matter? An Experimental Evaluation of the Relative Abundance and Decay Rates of Aquatic Environmental DNA.

Environmental DNA (eDNA) is increasingly used to monitor aquatic macrofauna. Typically, short mitochondrial DNA fragments are targeted because these should be relatively more abundant in the environment as longer fragments will break into smaller fragments over time. However, longer fragments may permit more flexible primer design and increase taxonomic resolution for eDNA metabarcoding analyses, and recent studies have shown that long mitochondrial eDNA fragments can be extracted from environmental water samples. Nuclear eDNA fragments have also been proposed as targets, but little is known about their persistence in the aquatic environment. Here we measure the abundance of mitochondrial eDNA fragments of different lengths and of short nuclear eDNA fragments, originating from captive fish in experimental tanks, and we test whether longer mitochondrial and short nuclear fragments decay faster than short mitochondrial fragments following fish removal. We show that when fish are present, shorter mitochondrial fragments are more abundant in water samples than both longer mitochondrial fragments and short nuclear eDNA fragments. However, the rate of decay following fish removal was similar for all fragment types, suggesting that the differences in abundance resulted from differences in the rates at which different fragment types were produced rather than differences in their decay rates.

Taxonomic similarity, more than contact opportunity, explains novel plant-pathogen associations between native and alien taxa.

Novel associations between plants and pathogens can have serious impacts on managed and natural ecosystems world-wide. The introduction of alien plants increases the potential for biogeographically novel plant-pathogen associations to arise when pathogens are transmitted from native to alien plant species and vice versa. We quantified biogeographically novel associations recorded in New Zealand over the last 150 yr between plant pathogens (fungi, oomycetes and plasmodiophorids) and vascular plants. We examined the extent to which taxonomic similarity, pathogen traits, contact opportunity and sampling effort could explain the number of novel associates for host and pathogen species. Novel associations were common; approximately one-third of surveyed plants and pathogens were recorded with at least one biogeographically novel associate. Native plants had more alien pathogens than vice versa. Taxonomic similarity between the native and alien flora and the total number of recorded associations (a measure of sampling effort) best explained the number of novel associates among species. The frequency of novel associations and the importance of sampling effort as an explanatory variable emphasize the need for effective monitoring and risk assessment tools to mitigate the potential environmental and economic impact of novel pathogen associations.

Salinized rivers: degraded systems or new habitats for salt-tolerant faunas?

Anthropogenic salinization of rivers is an emerging issue of global concern, with significant adverse effects on biodiversity and ecosystem functioning. Impacts of freshwater salinization on biota are strongly mediated by evolutionary history, as this is a major factor determining species physiological salinity tolerance. Freshwater insects dominate most flowing waters, and the common lotic insect orders Ephemeroptera (mayflies), Plecoptera (stoneflies) and Trichoptera (caddisflies) are particularly salt-sensitive. Tolerances of existing taxa, rapid adaption, colonization by novel taxa (from naturally saline environments) and interactions between species will be key drivers of assemblages in saline lotic systems. Here we outline a conceptual framework predicting how communities may change in salinizing rivers. We envision that a relatively small number of taxa will be saline-tolerant and able to colonize salinized rivers (e.g. most naturally saline habitats are lentic; thus potential colonizers would need to adapt to lotic environments), leading to depauperate communities in these environments.

Magnitude and variation of prehistoric bird extinctions in the Pacific.

The largest extinction event in the Holocene occurred on Pacific islands, where Late Quaternary fossils reveal the loss of thousands of bird populations following human colonization of the region. However, gaps in the fossil record mean that considerable uncertainty surrounds the magnitude and pattern of these extinctions. We use a Bayesian mark-recapture approach to model gaps in the fossil record and to quantify losses of nonpasserine landbirds on 41 Pacific islands. Two-thirds of the populations on these islands went extinct in the period between first human arrival and European contact, with extinction rates linked to island and species characteristics that increased susceptibility to hunting and habitat destruction. We calculate that human colonization of remote Pacific islands caused the global extinction of close to 1,000 species of nonpasserine landbird alone; nonpasserine seabird and passerine extinctions will add to this total.

Functional equivalence, competitive hierarchy and facilitation determine species coexistence in highly invaded grasslands.

Alien and native plant species often differ in functional traits. Trait differences could lead to niche differences that minimize competitive interactions and stabilize coexistence. However, trait differences could also translate into average fitness differences, leading to a competitive hierarchy that prevents coexistence. We tested whether trait differences between alien and native species translated into average fitness or stabilizing niche differences, and whether competition could explain observed coexistence within invaded grassland communities (New Zealand). Trait differences reflected marked competitive hierarchy, suggesting average fitness differences. Species coexistence was determined by a trade-off between species susceptibility to herbivory vs competitive hierarchy and facilitation. Importantly, although aliens and natives differed in their trait values, they did not differ in their competitive response, highlighting the importance of equalizing mechanisms in structuring invaded communities. Only a few alien species with a particular set of traits were able to jeopardize species coexistence when grazing was ceased. Our study explains why some alien species coexist with natives, whereas others have strong impacts on native communities. It highlights that trait differences can underlie several coexistence processes and that the demonstration of trait differences between aliens and natives is only a first step to understanding the role of biotic interactions in structuring invaded communities.

Quantifying invasion resistance: the use of recruitment functions to control for propagule pressure.

Invasive species distributions tend to be biased towards some habitats compared to others due to the combined effects of habitat-specific resistance to invasion and non-uniform propagule pressure. These two factors may also interact, with habitat resistance varying as a function of propagule supply rate. Recruitment experiments, in which the number of individuals recruiting into a population is measured under different propagule supply rates, can help us understand these interactions and quantify habitat resistance to invasion while controlling for variation in propagule supply rate. Here, we constructed recruitment functions for the invasive herb Hieracium lepidulum by sowing seeds at five different densities into six different habitat types in New Zealand's Southern Alps repeated over two successive years, and monitored seedling recruitment and survival over a four year period. We fitted recruitment functions that allowed us to estimate the total number of safe sites available for plants to occupy, which we used as a measure of invasion resistance, and tested several hypotheses concerning how invasion resistance differed among habitats and over time. We found significant differences in levels of H. lepidulum recruitment among habitats, which did not match the species' current distribution in the landscape. Local biotic and abiotic characteristics helped explain some of the between-habitat variation, with vascular plant species richness, vascular plant cover, and light availability, all positively correlated with the number of safe sites for recruitment. Resistance also varied over time however, with cohorts sown in successive years showing different levels of recruitment in some habitats but not others. These results show that recruitment functions can be used to quantify habitat resistance to invasion and to identify potential mechanisms of invasion resistance.

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.

Effects of spatially extensive control of invasive rats on abundance of native invertebrates in mainland New Zealand forests.

Predation on native fauna by non-native invasive mammals is widely documented, but effects of predation at the population level are rarely measured. Eradication of invasive mammals from islands has led to recovery of native biota, but the benefits of controlling invasive mammal populations in settings where eradication is not feasible are less understood. We used various combinations of aerially delivered toxic bait and control measures on the ground to reduce abundances of invasive rats (Rattus rattus) to low levels over large areas on mainland New Zealand and then monitored the abundance of invertebrates on replicated treatment sites to compare with abundances on similar nontreatment sites. We also assessed rat diet by examining stomach contents. Abundance of the rats' most-consumed invertebrate prey item, the large-bodied Auckland tree weta (Hemideina thoracica), increased 3-fold on treatment sites where we maintained rats at <4/ha for approximately 3 years, compared with the nontreatment sites. Auckland tree weta also increased in abundance on sites where rats were controlled with a single aerial-poisoning operation, but rat abundance subsequently increased on these sites and tree weta abundance then declined. Nevertheless, our data suggest that biennial reduction of rat abundances may be sufficient to allow increases in tree weta populations. Other invertebrates that were consumed less often (cave weta [Rhaphidophoridae], spiders [Araneae], and cockroaches [Blattodea]) showed no systematic changes in abundance following rat control. Our results suggest that the significant threat to recruitment and individual survival that predation by rats poses for tree weta can be mitigated by wide-scale aerial pest control.