Trailing-edge zombie forests can increase population persistence in the face of climate change

Climate-driven habitat shifts pose challenges for dispersal-limited, late-maturing taxa such as trees. Older trees are often the most reproductive individuals in the population, but as habitats shift, these individuals can be left behind in the trailing range edge, generating "zombie forests" that may persist long after the suitable habitat has shifted. Are these zombie forests vestiges of ecosystems past or do they play an ecological role? To understand how zombie forests affect population persistence, we developed a spatially explicit, stage-structured model of tree populations occupying a shifting habitat. Our model shows that seed dispersal from zombie forests to the range core can considerably increase the maximum rate of climate change that a population can withstand. Moreover, the entire core population can ultimately descend from recruitment-limited zombie forests, highlighting their demographic value. Our results suggest that preserving trailing-edge zombie forests can greatly increase population persistence in the face of climate change.

Genetic variability and the ecology of geographic range: a test of the central-marginal hypothesis in Australian scincid lizards

For many species, both local abundance and regional occupancy are highest near the center of their geographic distributions. One hypothesis for this pattern is that niche suitability declines with increasing distance from a species geographic center, such that populations near range margins are characterized by reduced density and increased patchiness. In these smaller edge populations, genetic drift is more powerful, leading to the loss of genetic diversity. This simple verbal model has been formalized as the central-marginal hypothesis, which predicts that core populations should have greater genetic diversity than edge populations. However, demographic shifts over time can generate a similar pattern. For example, in species with expanding ranges, populations at the range edge experience serial founder effects, creating a gradient of declining genetic diversity from the range core to edge. Testing the central-marginal hypothesis properly thus requires us to consider the confounding role of historical demography. Here, we account for the role of history in testing the central-marginal hypothesis using a genomic dataset of 25 species-level taxa of Australian skink lizards (genus: Ctenotus and Lerista). We found support for the central-marginal hypothesis in 16 of our 25 taxa, of which eight taxa recovered significant support. Unexpectedly, species with the strongest evidence for range expansion were the least likely to follow predictions of the central-marginal hypothesis. The majority of these species had range expansions that originated at the range edge, which led to lower genetic diversity at the range edge compared to the core, contrary to the central-marginal hypothesis.

Brain transcriptome analysis reveals gene expression differences associated with dispersal behaviour between range-front and range-core populations of invasive cane toads in Australia

Understanding the mechanisms underlying rapid adaptation of invasive species in novel environments is key to improving our ability to manage these species. Many invaders demonstrate rapid evolution of behavioural traits involved in range expansion such as locomotor activity, exploration and risk-taking. However, the molecular mechanisms that underpin these changes are poorly understood. In 86 years, invasive cane toads (Rhinella marina) in Australia have drastically expanded their geographic range westward from coastal Queensland to Western Australia. During their range expansion, toads have undergone extensive phenotypic changes, particularly in behaviours that enhance the toads' dispersal ability. Common-garden experiments have shown that some changes in behavioural traits related to dispersal are heritable. However, genetic diversity is greatly reduced across the invasive range due to a strong founder effect, and the genetic basis underlying dispersal-related behavioural changes remains unknown. Here we used RNA-seq to compare the brain transcriptomes of toads from the Hawai'ian source population, as well as three distinct populations from across the Australian invasive range. We found markedly different gene expression profiles between the source population and Australian toads. By contrast, cane toads from across the Australian invasive range had very similar transcriptomic profiles. Yet, key genes with functions putatively related to dispersal behaviour showed differential expression between range-core and range-front populations. These genes could play an important role in the behavioural changes characteristic of range expansion in Australian cane toads.

Genetically-based adaptive trait shifts at an expanding mangrove range margin

Many species are expanding beyond their distributional range margins in response to a warming planet. Due to marginal environmental conditions and novel selection pressures, range margins may foster unique genetic adaptations that can better enable species to thrive under the extreme climatic conditions at and beyond their current distributional limits. Neotropical black mangrove (Avicennia germinans) is expanding poleward into temperate salt marsh along Atlantic Florida, USA, with field evidence of adaptive trait shifts within range-margin A. germinans populations. However, whether these adaptive shifts have a genetic basis remains to be answered. We monitored twenty A. germinans maternal cohorts from areas in both the Atlantic Florida range core and margin in a greenhouse common garden with annual temperatures analogous to range-margin conditions. We measured variation in a series of phenotypic traits starting at initial planting of field-collected propagules and continuing until two years development. Maternal cohorts from the Atlantic Florida range margin consistently outperformed those from the range core throughout the experiment. Range-margin cohorts survived in greater numbers, established faster, and were less stressed under winter chilling and sub-zero temperatures that are often reached at the Atlantic range margin, but not within the range core. Range-margin cohorts did not grow taller, but instead invested more into lateral growth and biomass accumulation that presumably reflects adaptation to their colder and open canopy environment. Range-margin cohorts also exhibited leaf traits consistent with greater resource acquisition that may compensate for a shorter growing season and reduced light quality at higher latitude. Synthesis: We confirmed that there is a genetic basis to adaptive trait shifts towards an expanding mangrove range margin. Our results suggest that genetically-based phenotypic differences better enable these range-margin mangroves to thrive within their stressful environment and may facilitate further poleward expansion in the future. In addition, our documentation of adaptive trait variation among maternal cohorts of an ecologically-important mangrove foundation species, quantitative data that is lacking for mangroves, should help inform mangrove restoration initiatives.

Genetic similarity enhances the strength of the relationship between gut bacteria and host DNA methylation

Factors such as host age, sex, diet, health status and genotype constitute the environmental envelope shaping microbial communities in the host′s gut. It has also been proposed that gut microbiota may be influenced by host epigenetics. Although the relationship between the host′s genotype/epigenotype and its associated microbiota has been the focus of a number of recent studies, the relative importance of these interactions and their biological relevance are still poorly understood. We used methylation-sensitive genotyping by sequencing to genotype and epigenotype invasive cane toads (Rhinella marina) from the species′s Australian range-core (three sites) and the invasion-front (three sites), and 16S rRNA gene sequencing to characterize their gut bacterial communities. We tested the effect of host genotype and epigenotype (i.e., methylome) on gut bacterial communities. Our results indicate that the genotypes, epigenotypes and gut communities of the range-core and invasion-front are significantly different from one another. We found a positive association between host pairwise genetic and epigenetic distances. More importantly, a positive relationship was found between the host′s epigenetic and gut bacterial pairwise distances. Interestingly, this association was stronger in individuals with low genetic differentiation. Our findings suggest that in range-expanding populations, where individuals are often genetically similar, the interaction between gut bacterial communities and host methylome may provide a mechanism through which invaders increase the plasticity of their response to novel environments, potentially increasing their invasion success.

Host defense or parasite cue: Skin secretions mediate interactions between amphibians and their parasites

Amphibian skin secretions (substances produced by the amphibian plus microbiota) plausibly act as a first line of defense against pathogen attack, but may also provide chemical cues for pathogens. To clarify the role of skin secretions in host-parasite interactions, we conducted experiments using cane toads (Rhinella marina) and their lungworms (Rhabdias pseudosphaerocephala) from the range-core and invasion-front of the introduced anurans’ range in Australia. Depending on the geographic area, toad skin secretions can reduce the longevity and infection success of parasite larvae, or attract lungworm larvae and enhance their infection success. These striking differences between the two regions were due both to differential responses of the larvae, and differential effects of the skin secretions. Our data suggest that skin secretions play an important role in host-parasite interactions in anurans, and that the arms race between a host and parasite can rapidly generate spatial variation in critical features of that interaction.

The accelerating anuran: evolution of locomotor performance in cane toads ( Rhinella marina , Bufonidae) at an invasion front

As is common in biological invasions, the rate at which cane toads ( Rhinella marina ) have spread across tropical Australia has accelerated through time. Individuals at the invasion front travel further than range-core conspecifics and exhibit distinctive morphologies that may facilitate rapid dispersal. However, the links between these morphological changes and locomotor performance have not been clearly documented. We used raceway trials and high-speed videography to document locomotor traits (e.g. hop distances, heights, velocities, and angles of take-off and landing) of toads from range-core and invasion-front populations. Locomotor performance varied geographically, and this variation in performance was linked to morphological features that have evolved during the toads' Australian invasion. Geographical variation in morphology and locomotor ability was evident not only in wild-caught animals, but also in individuals that had been raised under standardized conditions in captivity. Our data thus support the hypothesis that the cane toad's invasion across Australia has generated rapid evolutionary shifts in dispersal-relevant performance traits, and that these differences in performance are linked to concurrent shifts in morphological traits.

Judging meaning: A domain-level difference between autistic and non-autistic adults

We tested whether autistic adults would show selective difficulties across several tests of inferencing and social understanding in the context of average-range core language ability. One-hundred and ninety-one participants completed an online battery, and data were analysed using confirmatory factor analysis. Results showed that vocabulary knowledge was separate from other measures, which collectively formed a ‘receptive communication' factor. Autistic people underperformed on the ‘receptive communication' factor but showed more advanced vocabulary knowledge than non-autistic participants. Lower performance among autistic adults on the test battery predicted face-to-face communication difficulties measured by self-report and researcher ratings, with moderate effect sizes. Follow-up analysis indicated three further findings. We hypothesized that differences would arise from an isolated ‘theory of mind' difficulty in autistic people, but instead the data suggested more general information-processing differences when making judgements about communicative stimuli. Second, substantial group differences on a test of implied meaning were only partly explained at the factor level, suggesting that multiple cognitive influences underpinned these differences. Finally, autistic women tended to perform better than autistic men. Our results support the idea of a subtle domain-level difference in pragmatics in autistic people, while questioning the basis of this difference and highlighting substantial variability in skills across groups.