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Rapid evolution of parasite life history traits on an expanding range-edge
Abstract
Ecology Letters (2012) 15 : 329–337
Abstract
Parasites of invading species undergoing range advance may be exposed to powerful new selective forces. Low host density in range‐edge populations hampers parasite transmission, requiring the parasite to survive longer periods in the external environment before encountering a potential host. These conditions should favour evolutionary shifts in offspring size to maximise parasite transmission. We conducted a common‐garden experiment to compare life history traits among seven populations of the nematode lungworm ( Rhabdias pseudosphaerocephala) spanning from the parasite population core to the expanding range‐edge in invasive cane toads ( Rhinella marina ) in tropical Australia. Compared to conspecifics from the population core, nematodes from the range‐edge exhibited larger eggs, larger free‐living adults and larger infective larvae, and reduced age at maturity in parasitic adults. These results support a priori predictions regarding adaptive changes in offspring size as a function of invasion history, and suggest that parasite life history traits can evolve rapidly in response to the selective forces exerted by a biological invasion.
... A native-range parasite, the nematode lungworm Rhabdias pseudosphaerocephala (hereafter lungworms), survived the toad's multiple translocations (26) and occurs across the Australian range of the toad. An arms-race has developed between toads and lungworms (27), resulting in toads from different parts of the invasive range having differential resistance to infection (30). Potential explanations for that spatial variation in vulnerability include differential skin permeability (28), attractiveness to lungworm larvae (29), or investment in immune responses (30) in toads from different areas. ...
... These results suggest that the major phase of host-parasite interactions affected by the arms race is the ability of lungworm larvae to travel through the host's body and establish infections in the lungs, rather than earlier phases such as recognising host presence through chemical cues or initiating attempts to penetrate the host's body. Consistent with our results, previous research has shown that blood plasma from range-edge (WA) toads is relatively ineffective at killing range-core worms (7), and that lungworms from the range-edge are larger than are those from other locations (27). Such local adaptation and differences in lungworm infectivity between populations may explain why range-edge toads are resistant to some populations (7), yet were susceptible to the NT lungworms used in this study. ...
... Changes in the evolved interaction between toads and their lungworm parasites appear to have been especially rapid at the toad invasion's range-edge in WA (7,29), likely because low population densities of hosts (toads) at the invasion front decrease rates of parasite transmission (27). As a result, selection for mounting an effective immune response to fight parasite attack may be weaker at the invasion front than elsewhere (consistent with the enemy release hypothesis: (45). ...
Evolutionary arms races can alter both parasite infectivity and host resistance, and it is difficult to separate the effects of these twin determinants of infection outcomes. Using a co-introduced, invasive host-parasite system (the lungworm Rhabdias pseudosphaerocephala and the cane toad Rhinella marina), we quantified behavioural responses of parasite larvae to skin-chemical cues of toads from different invasive populations, and rates at which hosts became infected following standardised exposure to lungworms. Chemical cues from toad skin altered host-seeking behaviour by parasites, similarly among populations. The number of infection attempts (parasite larvae entering the host’s body) also did not differ between populations, but rates of successful infection (establishment of adult worm in host lungs) was higher for range-edge toads than for range-core conspecifics. Thus, lower resistance to parasite infection in range-edge toads appears to be due to less effective immune defences of the host rather than differential behavioural responses of the parasite. In this ongoing host-parasite arms-race, changing outcomes appear to be driven by shifts in host immunocompetence.
... Biological invasions provide unparalleled opportunities to investigate arms races between hosts and their parasites, because they create spatial heterogeneity in transmission rates and impose novel selective forces on one or both participants (Lymbery et al., 2014). Recently, we showed that the invasion of cane toads (Rhinella marina, Figure 1) through tropical Australia has generated substantial spatial divergence in host-parasite interactions Kelehear et al., 2012;Mayer et al., 2021). The toads have carried with them a native-range nematode (Rhabdias pseudosphaerocephala, Figure 1) (Dubey & Shine, 2008;Selechnik et al., 2017) that can reduce viability of the host (Finnerty et al., 2018;Kelehear et al., 2011). ...
... The risk of parasite infection has been modified by the invasion process, with low population densities of hosts at the invasion-front reducing opportunities for parasite transfer among toads (Phillips et al., 2010). Apparently as a result, toads at the western invasion-front have evolved a greater resistance to parasite infection (Mayer et al., 2021), and R. pseudosphaerocephala close to the invasion-front have evolved a higher infectivity (Kelehear et al., 2012), continuing the arms race. That situation provides an ideal opportunity to investigate the biological role of anuran skin secretions in host-parasite interactions. ...
... These larvae mate to produce infective third-stage larvae (L3), which develop for 4-10 days (L2 stage) before breaking out of their mother's body and entering the soil (Baker, 1979). When an L3 larva locates a host, it pierces the epidermis and migrates through tissue to reach the lungs of the toad where it matures and feeds on blood from capillary beds (Kelehear et al., 2012). The entire life cycle takes 5-36 days (Kelehear et al., 2012). ...
Amphibian skin secretions (substances produced by the amphibian plus microbiota) plausibly act as a first line of defense against parasite/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 geographical 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. We investigated the role of skin secretions in host–parasite interactions, by infecting cane toads from the range‐core and invasion‐front of their introduced range in Australia with lungworm parasites. Depending on the geographical area, toad skin secretions reduced the longevity and infection success of parasite larvae, or attracted lungworm larvae and enhanced their infection success. These striking differences between the two regions suggest that skin secretions play an important role in host–parasite interactions, and that the arms race between host and parasite can rapidly generate spatial variation in critical features of that interaction.
... Assuming a classic virulencetransmission trade-off (May & Anderson 1983;Bull 1994) and local feedbacks between epidemiology and selection, several models predict that more virulent parasites will evolve in highly connected 'small-world' landscapes (Boots et al. 2004;Kamo & Boots 2006;Kamo et al. 2007) or at the front of advancing epidemics (Griette et al. 2015), where transmission is not limited by local depletion of susceptible hosts ('selfshading'). These predictions are consistent with observed changes in parasites of amphibian species (Kelehear et al. 2012;Phillips & Puschendorf 2013). ...
... It also relates to recent work on invasive species and range expansions, where dispersal evolution plays a key role in determining the rate of spatial diffusion (Kubisch et al. 2014). Hence, parasites may evolve 'invasion syndromes', with characteristic changes in life-history or transmission strategies (Kelehear et al. 2012;Phillips & Puschendorf 2013;Dunn & Hatcher 2015), thereby creating a positive feedback loop between rates of dispersal and rates of spatial spread of infection. ...
... Our evidence is robust, regardless of the data used for inference, which includes both direct experimental results as well as indirect estimates obtained by fitting an epidemiological model to time series. These results contrast with observations in certain natural epidemics (Kelehear et al. 2012), while confirming others (de Roode et al. 2008;Hawley et al. 2013). Our work calls for more detailed investigations of the role of infected host dispersal for epidemic spread and its implications for parasite lifehistory and virulence evolution. ...
Exploitative parasites are predicted to evolve in highly connected populations or in expanding epidemics. However, many parasites rely on host dispersal to reach new populations, potentially causing conflict between local transmission and global spread. We performed experimental range expansions in interconnected microcosms of the protozoan Paramecium caudatum, allowing natural dispersal of hosts infected with the bacterial parasite Holospora undulata. Parasites from range front treatments facilitated host dispersal and were less virulent, but also invested less in horizontal transmission than parasites from range cores. These differences were consistent with parameter estimates derived from an epidemiological model fitted on population‐level time‐series data. Our results illustrate how dispersal selection can have profound consequences for the evolution of parasite life history and virulence. Decrypting the eco‐evolutionary processes that shape parasite 'dispersal syndromes' may be important for the management of spreading epidemics in changing environments, biological invasions or in other spatial non‐equilibrium settings.
... After the toad defecates, these larvae mate to produce infective third-stage larvae (L3), which develop inside their mothers (Baker, 1979). When an L3 locates a host, it pierces the epidermis and migrates through tissue to reach the lungs of the toad, where it matures and feeds on blood from capillary beds (Kelehear et al., 2012). ...
... The westward invasion of the toad has also taken it from relatively equable climates to seasonally arid landscapes, where moist substrates (critical for survival of lungworm larvae) are scarce for most of the year. In response to the challenge of surviving in the external environment long enough to encounter a new host, the lungworm larvae at the invasion front are larger and more transmissible than those from long-established sites (Kelehear et al., 2012;Finnerty et al., 2018). In addition to low parasite density near the expanding edge of the range, it is plausible that the strains that occur there are less virulent than those from long-established populations, because increased transmissibility might be traded off against lowered virulence (Ewald, 1994). ...
... In addition to low parasite density near the expanding edge of the range, it is plausible that the strains that occur there are less virulent than those from long-established populations, because increased transmissibility might be traded off against lowered virulence (Ewald, 1994). In addition, spatial sorting of parasite phenotypes might accumulate less virulent strains at the invasion front because they are less likely to reduce the dispersal rate of their hosts (Kelehear et al., 2012). If parasite density and virulence are lower at invasion fronts, hosts in these locations are expected to invest less in resistance, because encounters with parasites are rare and the consequences of infection less serious. ...
By perturbing co-evolved interactions, biological invasions provide an opportunity to study the evolution of interactions between hosts and their parasites on ecological timescales. We studied the interaction between the cane toad (Rhinella marina) and its direct-lifecycle lungworm (Rhabdias pseudosphaerocephala) that was brought from South America to Australia with the toads in 1935. Compared with infective parasite larvae from long-established (range-core) toad populations, parasite larvae from toads near the invasion front were larger, lived longer and were better able to resist exposure to toxin from the parotoid glands of toads. Experimentally, we infected the common-garden-reared progeny of toads from range-core and invasion-front populations within Australia with lungworms from both populations. Infective larvae from invasion-front (vs. range-core) populations of the parasite were more successful at entering toads (by skin penetration) and establishing infections in the lungs. Toads from invasion-front populations were less prone to infection by either type of larvae. Thus, within 84 years, parasites at an invasion front have increased infectivity, whereas hosts have increased resistance to parasite infection compared with range-core populations. Rapid evolution of traits might affect host–parasite interactions during biological invasions, generating unpredictable effects both on the invaders and on native ecosystems.
... After the toad defecates, these larvae mate to produce infective third-stage larvae (L3), which develop inside their mothers (Baker, 1979). When an L3 locates a host, it pierces the epidermis and migrates through tissue to reach the lungs of the toad, where it matures and feeds on blood from capillary beds (Kelehear et al., 2012). ...
... The westward invasion of the toad has also taken it from relatively equable climates to seasonally arid landscapes, where moist substrates (critical for survival of lungworm larvae) are scarce for most of the year. In response to the challenge of surviving in the external environment long enough to encounter a new host, the lungworm larvae at the invasion front are larger and more transmissible than those from long-established sites (Kelehear et al., 2012;Finnerty et al., 2018). In addition to low parasite density near the expanding edge of the range, it is plausible that the strains that occur there are less virulent than those from long-established populations, because increased transmissibility might be traded off against lowered virulence (Ewald, 1994). ...
... In addition to low parasite density near the expanding edge of the range, it is plausible that the strains that occur there are less virulent than those from long-established populations, because increased transmissibility might be traded off against lowered virulence (Ewald, 1994). In addition, spatial sorting of parasite phenotypes might accumulate less virulent strains at the invasion front because they are less likely to reduce the dispersal rate of their hosts (Kelehear et al., 2012). If parasite density and virulence are lower at invasion fronts, hosts in these locations are expected to invest less in resistance, because encounters with parasites are rare and the consequences of infection less serious. ...
By perturbing co-evolved interactions, biological invasions provide an opportunity to study the evolution of interactions between hosts and their parasites on ecological timescales. We studied the interaction between the cane toad (Rhinella marina) and its direct-lifecycle lungworm (Rhabdias pseudosphaerocephala) that was brought from South America to Australia with the toads in 1935. Compared with infective parasite larvae from long-established (range-core) toad populations, parasite larvae from toads near the invasion front were larger, lived longer and were better able to resist exposure to toxin from the parotoid glands of toads. Experimentally, we infected the common-garden-reared progeny of toads from range-core and invasion-front populations within Australia with lungworms from both populations. Infective larvae from invasion-front (vs. range-core) populations of the parasite were more successful at entering toads (by skin penetration) and establishing infections in the lungs. Toads from invasion-front populations were less prone to infection by either type of larvae. Thus, within 84 years, parasites at an invasion front have increased infectivity, whereas hosts have increased resistance to parasite infection compared with range-core populations. Rapid evolution of traits might affect host-parasite interactions during biological invasions, generating unpredictable effects both on the invaders and on native ecosystems.
... Assuming a classic virulencetransmission trade-off (May & Anderson 1983;Bull 1994) and local feedbacks between epidemiology and selection, several models predict that more virulent parasites will evolve in highly connected 'small-world' landscapes (Boots et al. 2004;Kamo & Boots 2006;Kamo et al. 2007) or at the front of advancing epidemics (Griette et al. 2015), where transmission is not limited by local depletion of susceptible hosts ('selfshading'). These predictions are consistent with observed changes in parasites of amphibian species (Kelehear et al. 2012;Phillips & Puschendorf 2013). ...
... It also relates to recent work on invasive species and range expansions, where dispersal evolution plays a key role in determining the rate of spatial diffusion (Kubisch et al. 2014). Hence, parasites may evolve 'invasion syndromes', with characteristic changes in life-history or transmission strategies (Kelehear et al. 2012;Phillips & Puschendorf 2013;Dunn & Hatcher 2015), thereby creating a positive feedback loop between rates of dispersal and rates of spatial spread of infection. ...
... Our evidence is robust, regardless of the data used for inference, which includes both direct experimental results as well as indirect estimates obtained by fitting an epidemiological model to time series. These results contrast with observations in certain natural epidemics (Kelehear et al. 2012), while confirming others (de Roode et al. 2008;Hawley et al. 2013). Our work calls for more detailed investigations of the role of infected host dispersal for epidemic spread and its implications for parasite lifehistory and virulence evolution. ...
... While it is safe to assume that selection pressures will be asymmetric between hosts and parasites, the response of hosts and parasites will depend on how trait values of hosts (resistance, tolerance) and parasites (infectivity, transmission, virulence) can be translated into fitness in each specific case. Traits associated with infectivity (Weclawski et al., 2013;Weclawski et al., 2014) and transmission (Kelehear et al., 2012) were shown to evolve rapidly in invasive parasite populations. Evolution of both traits reflects selection pressures due to low host density (Phillips et al., 2010) that translates into longer periods of free-living infectious stages spent outside the host. ...
... Evolution of both traits reflects selection pressures due to low host density (Phillips et al., 2010) that translates into longer periods of free-living infectious stages spent outside the host. Survival of infective stages can therefore evolve rapidly (Kelehear et al., 2012). ...
... Besides co-introducing parasites to their new range, invasive hosts are also often confronted with native parasites in the introduced range that will exert selection on the invader (e.g. Kelehear et al., 2012). Rapid evolution of host resistance against these newly encountered parasites will increase host fitness and may be a decisive factor prolonging invasion success. ...
... The free-living stage in the soil (L2) reproduces sexually. After mating, the males die and females develop one to four live offspring inside them [21,[24][25][26]. These offspring consume the mother's organs and burst through her cuticle into the soil as nonfeeding infective larvae (L3). ...
... Although selection and spatial sorting of dispersal-enhancing traits have altered immune investment of toads at the range edge [14,39,40], toads from the invasion front retained effective immune defences against lungworms from long-colonized areas (figure 2). The high infection success of invasion-front lungworms (consistent with earlier studies: [18,19,25]) cannot be explained by larger larvae, because the sizes of L3 used for experimental infections did not differ significantly among states. Instead, the higher infection abundances of invasionfront lungworms may result from circumstances that intensify selection on the ability of parasites to infect new hosts. ...
By imposing novel selection pressures on both participants, biological invasions can modify evolutionary ‘arms races’ between hosts and parasites. A spatially replicated cross-infection experiment reveals strong spatial divergence in the ability of lungworms (Rhabdias pseudosphaerocephala) to infect invasive cane toads (Rhinella marina) in Australia. In areas colonized for longer than 20 years, toads are more resistant to infection by local strains of parasites than by allopatric strains. The situation reverses at the invasion front, where super-infective parasites have evolved. Invasion-induced shifts in genetic diversity and selective pressures may explain why hosts gain advantage over parasites in long-colonized areas, whereas parasites gain advantage at the invasion front.
... These lungworms can reduce rates of feeding, growth, and survival in cane toads (Kelehear et al. 2011;Finnerty et al. 2018) and are absent from the invasion front because infected toads exhibit lower dispersal rates (Phillips et al. 2010b). Lungworms A c c e p t e d M a n u s c r i p t from populations closer to the invasion front have evolved larger egg size and accelerated maturation, relative to lungworms in long-colonised areas (Kelehear et al. 2012;Schlippe Justicia et al. 2022). Cross-infection experiments reveal that the ability of a toad to resist infection, and the ability of lungworm larvae to infect a new host, differ considerably among geographic host-parasite combinations (Mayer et al. 2021). ...
... -Toads near the invasion front invest less in immune defence (Llewellyn et al. 2012) and modify the form of that investment . Also, at least one major parasite (a nematode lungworm brought with the toad from South America) has evolved changes in traits such as egg size and time to maturity (Kelehear et al. 2012). As a result, toads from different regions of Australia are differentially vulnerable to lungworms from different regions. ...
Natural populations can show rapid adaptive responses to intense (human-mediated) environmental change. The potential for exploiting rapidly evolved traits for conservation management has been often discussed but rarely implemented. Capitalizing on a well-studied biological invasion, we here explore the idea that rapid phenotypic change in the invaders, their pathogens, and the native biota provide opportunities for managers to control invader abundance and buffer adverse impacts on native wildlife. Intensive studies of the invasion of tropical Australia by cane toads (Rhinella marina) have identified newly-evolved vulnerabilities that we could exploit for toad control; and newly-evolved resilience of native wildlife that we could exploit for impact reduction. For example, distinctive phenotypes of toads at the expanding range edge enhance dispersal rate but reduce reproductive output, intraspecific competitive ability and immunocompetence; and the evolution of larval cannibalism creates opportunities not only for species-specific trapping of toad tadpoles, but also could be exploited (when allied to emerging CRISPR-Cas9 techniques) to intensify intraspecific conflict in invasive toads. That is, we could use the invasive species to control their own populations. This case study illustrates the potential of detailed basic research to identify novel approaches for conservation.
... prevalence at I. ricinus range margins may enhance population growth and competitive ability of hosts and vectors. Less infected, hosts may, for example, invest differently in immunity and reproduction than hosts in core populations [15,54], which can affect hostparasite interactions when the parasite finally invades host populations at the range margins [55]. A better understanding of eco-evolutionary processes between pathogens, vectors and hosts at range margins, and their effect on pathogen life-history and virulence evolution, will therefore be a fruitful next step (e.g. ...
... A better understanding of eco-evolutionary processes between pathogens, vectors and hosts at range margins, and their effect on pathogen life-history and virulence evolution, will therefore be a fruitful next step (e.g. [55]), and will contribute to a better prediction of zoonotic disease risks in regions where vectors and pathogens are newly emerging due to climate change. ...
Background
Parasites can alter host and vector phenotype and thereby affect ecological processes in natural populations. Laboratory studies have suggested that Borrelia burgdorferi sensu lato, the causative agent of human Lyme borreliosis, may induce physiological and behavioural alterations in its main tick vector in Europe, Ixodes ricinus , which increase the tick’s mobility and survival under challenging conditions. These phenotypic alterations may allow I. ricinus to colonise marginal habitats (‘facilitation hypothesis’), thereby fuelling the ongoing range expansion of I. ricinus towards higher elevations and latitudes induced by climate change. To explore the potential for such an effect under natural conditions, we studied the prevalence of B. burgdorferi s.l. in questing I. ricinus and its variation with elevation in the Swiss Alps.
Results
We screened for B. burgdorferi s.l. infection in questing nymphs of I. ricinus (N = 411) from 15 sites between 528 and 1774 m.a.s.l to test if B. burgdorferi s.l. prevalence is higher at high elevations (i.e. in marginal habitats). Opposite of what is predicted under the facilitation hypothesis, we found that B. burgdorferi s.l. prevalence in I. ricinus nymphs decreased with increasing elevation and that Borrelia prevalence was 12.6% lower in I. ricinus nymphs collected at the range margin compared to nymphs in the core range. But there was no association between Borrelia prevalence and elevation within the core range of I. ricinus . Therefore the observed pattern was more consistent with a sudden decrease in Borrelia prevalence above a certain elevation, rather than a gradual decline with increasing elevation across the entire tick range.
Conclusions
In conclusion, we found no evidence that B. burgdorferi s.l.-induced alterations of I. ricinus phenotype observed in laboratory studies facilitate the colonisation of marginal habitats in the wild. Rather, ticks in marginal habitats are substantially less likely to harbour the pathogen. These findings have implications for a better understanding of eco-evolutionary processes in natural host-parasite systems, as well as the assessment of Lyme borreliosis risk in regions where I. ricinus is newly emerging.
... A native-range parasite, the nematode lungworm Rhabdias pseudosphaerocephala (hereafter lungworms), survived the toad's multiple translocations [26] and occurs across the Australian range of the toad. An arms race has developed between toads and lungworms [27]. Range-front toads reduce investment in immune defences [28] but can be more resistant to infection from lungworms [7,29]. ...
... Toads at the range-edge thus may be exposed to different kinds of lungworms, as well as fewer of them, favouring investment into different kinds of immune defences such as eosinophils, macrophages or inflammation. Changes in the evolved interaction between toads and their lungworm parasites appear to have been especially rapid at the toad invasion's range-edge in WA [7,29], likely because of low population densities of hosts (toads) at the invasion front decrease rates of parasite transmission [27]. As a result, selection for mounting an effective immune response to fight parasite attack may be weaker at the invasion front than elsewhere (consistent with the enemy release hypothesis [46]). ...
Evolutionary arms races can alter both parasite infectivity and host resistance, and it is difficult to separate the effects of these twin determinants of infection outcomes. We used a co-introduced, invasive host-parasite system (the lungworm Rhabdias pseudosphaerocephala and cane toads Rhinella marina), where rapid adaptation and dispersal have led to population differences in infection resistance. We quantified behavioural responses of parasite larvae to skin-chemical cues of toads from different invasive populations, and rates at which juvenile hosts became infected following standardized exposure to lungworms. Chemical cues from toad skin altered host-seeking behaviour by parasites, similarly among populations. The number of infection attempts (parasite larvae entering the host's body) also did not differ between populations, but rates of successful infection (establishment of adult worm in host lungs) were higher for range-edge toads than for range-core conspecifics. Thus, lower resistance to parasite infection in range-edge juvenile toads appears to be due to less effective immune defences of the host rather than differential behavioural responses of the parasite. In this ongoing host-parasite arms race, changing outcomes appear to be driven by shifts in host immunocompetence.
... Next to high plasticity (Richards et al., 2006;Knop and Reusser, 2012), rapid adaptation to new environmental and ecological conditions can increase fitness and several studies have shown rapid adaptation of fitness relevant traits after colonization (Dlugosch and Parker, 2008). Among others, these included adaptations to climatic conditions (Colautti and Barrett, 2013;Colautti and Lau, 2015) as well as coevolution in novel biotic interactions of hosts and parasites (Kelehear et al., 2012;Weclawski et al., 2013;Wendling and Wegner, 2015;Feis et al., 2016;Goedknegt et al., 2016). In these cases adaptation was deduced from phenotypic differences comparing native and invasive populations (Weclawski et al., 2013) or trajectories along invasions fronts (Kelehear et al., 2012;Colautti and Barrett, 2013;Feis et al., 2016) leaving the underlying adaptive changes on the genetic level unresolved. ...
... Among others, these included adaptations to climatic conditions (Colautti and Barrett, 2013;Colautti and Lau, 2015) as well as coevolution in novel biotic interactions of hosts and parasites (Kelehear et al., 2012;Weclawski et al., 2013;Wendling and Wegner, 2015;Feis et al., 2016;Goedknegt et al., 2016). In these cases adaptation was deduced from phenotypic differences comparing native and invasive populations (Weclawski et al., 2013) or trajectories along invasions fronts (Kelehear et al., 2012;Colautti and Barrett, 2013;Feis et al., 2016) leaving the underlying adaptive changes on the genetic level unresolved. ...
Upon colonizing new habitats, invasive species face a series of new selection pressures as a result of changing abiotic conditions and novel biotic interactions with native species. These new selection pressures can be accommodated by different mechanisms that act on different levels and across different time scales: (1) By changing transcriptomic profiles, species can react by plasticity within individual physiological limitations. (2) Invasive populations can adapt by fixing beneficial genetic variants in response to the newly encountered selection pressures. Here, we compare the genomic and transcriptomic landscapes of two independent invasions of the Pacific Oyster (Crassostrea gigas) into the North Sea. In detail, we combine ddRAD sequencing on the genomic level with RNAseq on the transcriptomic level to reveal outlier loci (SNPs) indicative of adaptation, as well as transcriptomic profiles from a translocation experiment to show immediate physiological reactions between two populations characterizing the two independent invasions. Generally, we found low physical congruence between differentially regulated genes and outlier loci, indicating that different genes are involved on the different time scales. Functionally matching outlier loci and differentially expressed genes were however found for spliceosomal modification of mRNA and particularly for transposon activation, indicating that these variation creating processes might be connected across eco-physiological and evolutionary time scales. By contrasting and identifying functional congruence between population outlier loci and population specific transcriptomic profiles, we can thus reveal a glimpse at the traits and processes characterizing specific mechanisms involved in successful invasions.
... (Kelehear et al. 2009Kelehear et al. , 2011Phillips et al. 2010;Pizzatto & Shine 2012a;Tingley et al. 2017). Although many aspects of the cane toad–Rhabdias system, such as distribution and infection dynamics, are well understood (Pizzatto et al. 2010Pizzatto et al. , 2012Kelehear et al. 2011;Kelehear, Brown & Shine 2012a), considerable ambiguity remains regarding the effect of the parasite on host fitness. Previous experimental studies have focused on metamorphs rather than adult toads (Kelehear et al. 2009;Pizzatto et al. 2010), or have been based on captive or correlational studies (Kelehear et al. 2011). ...
... If so, the effects of lungworms may be more devastating for toads at the invasion front than is the case in the already-colonised areas in which we studied these interactions. By the same token, virulence of the parasite may have diminished at the invasion front (Phillips et al. 2010;Kelehear et al. 2012a). Thus, exposing naïve invasionfront toads to more virulent parasites from long-established populations may result in even ...
Most research on the effects of parasites on their hosts has focused on the parasites of mammals or birds (especially, domesticated taxa) rather than systems in which the hosts are ectothermic wildlife species.
We used experimental methods (antihelminthic drugs) to quantify the effects of lungworms ( Rhabdias pseudosphaerocephala ) on their anuran hosts, the invasive cane toad ( Rhinella marina ).
In captivity, eradicating lungworms enhanced toad activity (measures of boldness and level of spontaneous activity), performance (locomotor speed, climbing ability) and foraging success (feeding rate).
In free‐ranging toads ( n = 123) at a site in tropical Australia, eradicating lungworm infection increased rates of host survival by 8%, movement by 20%, growth by 28% and elaboration of male secondary sexual characteristics by 30%. The presence of the lungworm thus has a substantial negative effect on fitness‐related traits of the host.
Given their long shared evolutionary history and the mild inflammatory and immune response elicited by the parasite in the host, the magnitude of the effects of parasite removal were surprising. Parasites may impose hidden costs, related to modification of host behaviour or metabolism. Experimental removal of parasites can be a useful means of quantifying costs of infection.
A plain language summary is available for this article.
... For parasites, a decrease in host density should signify a lower probability of transmission, a new pressure that could shift the optimal reproductive strategy along this continuum. For example, populations of the nematode Rhabdias pseudosphaerocephala have evolved larger eggs, larger infective larvae and a reduced age at maturity along the edges of the expanding spatial range of their host, the invasive cane toad Rhinella marina, in Australia, where host densities are much lower than those in the centre of the host range (Kelehear, Brown & Shine, 2012). These new lifehistory traits have evolved rapidly, better equipping the parasite's eggs and larvae to survive the longer periods in the external environment they endure before encountering a host in conditions of low host density. ...
The Anthropocene is seeing the human footprint rapidly spreading to all of Earth's ecosystems. The fast‐changing biotic and abiotic conditions experienced by all organisms are exerting new and strong selective pressures, and there is a growing list of examples of human‐induced evolution in response to anthropogenic impacts. No organism is exempt from these novel selective pressures. Here, we synthesise current knowledge on human‐induced evolution in eukaryotic parasites of animals, and present a multidisciplinary framework for its study and monitoring. Parasites generally have short generation times and huge fecundity, features that predispose them for rapid evolution. We begin by reviewing evidence that parasites often have substantial standing genetic variation, and examples of their rapid evolution both under conditions of livestock production and in serial passage experiments. We then present a two‐step conceptual overview of the causal chain linking anthropogenic impacts to parasite evolution. First, we review the major anthropogenic factors impacting parasites, and identify the selective pressures they exert on parasites through increased mortality of either infective stages or adult parasites, or through changes in host density, quality or immunity. Second, we discuss what new phenotypic traits are likely to be favoured by the new selective pressures resulting from altered parasite mortality or host changes; we focus mostly on parasite virulence and basic life‐history traits, as these most directly influence the transmission success of parasites and the pathology they induce. To illustrate the kinds of evolutionary changes in parasites anticipated in the Anthropocene, we present a few scenarios, either already documented or hypothetical but plausible, involving parasite taxa in livestock, aquaculture and natural systems. Finally, we offer several approaches for investigations and real‐time monitoring of rapid, human‐induced evolution in parasites, ranging from controlled experiments to the use of state‐of‐the‐art genomic tools. The implications of fast‐evolving parasites in the Anthropocene for disease emergence and the dynamics of infections in domestic animals and wildlife are concerning. Broader recognition that it is not only the conditions for parasite transmission that are changing, but the parasites themselves, is needed to meet better the challenges ahead.
... Infectious disease should therefore become an important consideration in managing amphibian invasions. Importantly, numerous studies fell outside the direct scope of our review because they did not examine resident amphibians, with many of these studies documenting that invasive species were minimally impacted by pathogens in their non-native range (e.g., Hanselmann et al., 2004;Kelehear et al., 2012;Marr et al., 2010;Selechnik et al., 2017). In the few instances of IDR, the positive effects on native hosts were minimal. ...
Invasive species can influence host-pathogen dynamics through a variety of mechanisms, potentially exacerbating or ameliorating disease consequences for native species. Pathogenic infections influence amphibian population and community dynamics worldwide, to the extent that community composition is often structured by host-pathogen interactions. Multiple amphibian species have also invaded new environments globally, causing direct and potential indirect impacts on host and pathogen community composition. To synthesize knowledge on the consequences of invasive amphibians interacting with pathogens in novel environments, we systematically reviewed the current literature and quantified how invasive amphibian species alter disease dynamics within amphibian communities. Overall, we found 145 studies that assessed pathogen impacts of amphibian invasions. Of those, 110 documented invasion-facilitated disease amplification (IDA), where amphibian invaders increased pathogen diversity, prevalence, infection intensity, or decreased host fitness from pathogen infections. In contrast, 17 studies found no change on pathogens in the native community when an invasive amphibian arrived, and 19 studies documented invasion-facilitated disease reduction (IDR) in the resident amphibian community, where invasive species decreased negative pathogen impacts to native species. Thus, IDA was more common, and the magnitude of IDA effects was also larger than the minimal IDR effects observed. Finally, we identified gaps in the current literature and suggest management actions that may help to protect native amphibians from these negative interactions. Enhancing our knowledge of how invasive amphibian species interact with pathogens will improve the response to ongoing and future invasions in an era of global change that continues to drastically reduce global amphibian biodiversity.
... Second, specific biological knowledge is often vital for the development of effective management protocols (Donlan et al. 2003;Hoffmann 2015), especially idiosyncrasies of species that make them susceptible to management actions (Simberloff 2003). It is often important that this knowledge is gained on-site because the biology and ecology of species can vary greatly between the native and exotic range, as well as among exotic ranges (Bøhn et al. 2004;Wilder et al. 2011;Kelehear et al. 2012). For example, the northern tamarisk beetle Diorhabda carinulata, introduced into North America as a biocontrol agent against Tamarix spp. was effective in some regions, on some species, but failed in others (Bean et al. 2007). ...
... Helminth parasites can infect their hosts through direct contact of the larvae or through intermediate hosts. Infection parameters (e.g., abundance, prevalence) can be affected by aspects such as diet (Silva et al. 2019), microhabitat use (Brito et al. 2014) and host density (Kelehear et al. 2012), and these factors can be affected by environmental alterations, such as the agricultural land use (Portela et al. 2020). Among the problems that agricultural land use can cause in helminths, for example, are the reduction in the immune response or competence of the hosts (Kiesecker 2002), changes in habitat (Sillero et al. 2020) and changes in resource availability (Becker et al. 2015) that may imply changes in parasitism patterns (Brito et al. 2014;Becker et al. 2015;Kiesecker 2002). ...
Among the forms of anthropogenic disturbance, agricultural land use is one of the main threats to biodiversity. Understanding how interactions between parasites and hosts are affected by agricultural land use allows predictions of how these anthropogenic impacts affect parasites. Although parasitism patterns are affected by agricultural land use, it is noteworthy that different groups of parasites can respond differently to these environmental alterations. While heteroxenous species need more than one host to complete their life cycle and tend to be more harmed by anthropization, monoxenous species, which need only one host to complete their life cycle, tend to be less harmed. In this work, we evaluate how agricultural land use affects the abundance and prevalence of parasitism for monoxenous and heteroxenous helminths in the generalist lizard Tropidurus hispidus in Caatinga Domain, Brazil. We recorded differences in abundance and prevalence of heteroxeneous (higher in conserved areas) and monoxenous helminths (higher in agricultural areas). Heteroxenous helminths that have lizards as definitive hosts are mainly obtained through diet. Tropidurus hispidus predominantly consumes insects, so it is possible that the lower abundance and prevalence of heteroxenous parasites in agricultural areas, beyond habitat simplification, is related to the decrease in the insect population. As monoxenous species do not need an intermediate host, it is possible that this aspect has influenced their greater success in anthropogenic environments than heteroxenous species. This contrasting result reinforces the need for a separate assessment between these groups when evaluating effects of land use.
... This process has been proposed as a new evolutionary mechanism called "spatial sorting" (Shine et al, 2011;Phillips & Perkins, 2019). Researchers also found that parasite that infects range-expanding hosts will itself be subjected to spatial sorting (Shine et al, 2011), and its improved ability to successfully infect hosts is favored during this evolutionary process (Kelehear et al, 2012). Considering that viruses are obligate parasites and copropagate with their hosts, one could intuitively speculate that viruses that infect a range-expanding host will experience the same evolutionary process with the host, that is, the evolutionary changes of viruses mostly accumulating at the front of host expansion. ...
Current strategies to improve the throughput of continuous directed evolution technologies often involve complex mechanical fluid-controlling system or robotic platforms, which limits their popularization and application in general laboratories. Inspired by our previous study on bacterial range expansion, in this study, we report a system termed SPACE for rapid and extensively parallelizable evolution of biomolecules by introducing spatial dimensions into the landmark phage-assisted continuous evolution system. Specifically, M13 phages and chemotactic Escherichia coli cells were closely inoculated onto a semisolid agar. The phages came into contact with the expanding front of the bacterial range, and then comigrated with the bacteria. This system leverages competition over space, wherein evolutionary progress is closely associated with the production of spatial patterns, allowing the emergence of improved or new protein functions. In a prototypical problem, SPACE remarkably simplified the process and evolved the promoter recognition of T7 RNA polymerase (RNAP) to a library of 96 random sequences in parallel. These results establish SPACE as a simple, easy to implement, and massively parallelizable platform for continuous directed evolution in general laboratories.
... High population growth rates and short generation times of parasites [17] and parasite-transmitting vectors [57] are likely to promote thermal adaptation. This adaptive potential is seen in nematode lungworms (Rhabdias pseudosphaerocephala) that infect the invasive cane toad (Rhinella marina)lungworms produce larger eggs, larvae, and adults in host populations at the edge of their geographic range than within the optimal conditions of the range [58]. ...
The persistence of parasite populations through harsh seasonal bouts is often critical to circannual disease outbreaks. Parasites have a diverse repertoire of phenotypes for persistence, ranging from transitioning to a different life stage better suited to within-host dormancy to utilizing weather-hardy structures external to hosts. While these adaptive traits allow parasite species to survive through harsh seasons, it is often at survival rates that threaten population persistence. We argue that these periods of parasite (and vector) population busts could be ideal targets for disease intervention. As climate change portends abbreviated host dormancy and extended transmission periods in many host–parasite systems, it is essential to identify novel pathways to shore up current disease-intervention strategies.
... In particular, we found higher parasite species richness, abundance, mean intensity of infestation, prevalence, and co-infections in the urbanized area, including a higher presence of accidental parasites. While other studies have analyzed specific parasites (e.g., Rhabdias pseudosphaerocephala, Kelehear et al., 2012a; Raillietiella frenatus, Kelehear et al., 2012b) and their relationship with Rhinella under selective environmental pressures, there is little information regarding the role of urban disturbance in altering parasite diversity and interactions in this species and other amphibians in general. ...
... Host-parasite coevolution during invasion could also be disrupted by progressive shifts in traits related to the low density and enhanced dispersal ability of hosts at the expanding range edge Kelehear et al., 2012;Nørgaard et al., 2019aNørgaard et al., , 2021Phillips & Puschendorf, 2013). Because density of hosts is low at the range edge, selection may favor increased infectivity of the parasite, which, in turn, might result in increased resistance among toads at the invasion front to counter the increased infectivity of local lungworms . ...
Abstract Coevolutionary host–parasite “arms races” can be disrupted by new evolutionary forces imposed by biological invasions, affecting both host and parasite densities, as well as their traits. The spread of cane toads (Rhinella marina) and their parasitic lungworm (Rhabdias pseudosphaerocephala) across tropical Australia provides an ideal opportunity to study a perturbed host–parasite system. We conducted a cross‐infection experiment using common‐garden‐reared toads and lungworms from three regions (comprising long‐established, intermediate, and recently invaded sites across tropical Australia) to quantify traits of the parasite (infectivity and virulence) and the host (resistance and tolerance). Specifically, we assessed whether patterns of host–parasite co‐adaptation were better explained by spatial distances versus time since the separation of host and parasite populations. Infection success was highest when toads from long‐established populations were exposed to lungworms from close to the invasion front and lowest when frontal toads were exposed to parasites from older populations. This suggests that both parasite infectivity and host resistance have increased over the course of invasion. In contrast, most virulence/tolerance traits have not consistently increased or decreased during invasion. Higher parasite burdens were associated with increased feeding performance in toads and faster growth in lungworms, counter‐intuitive results that suggest host manipulation by the parasite.
... However, other systems, such as captive host populations either inside or outside their natural species ranges (e.g., Milotic et al. 2020), or hosts in ephemeral habitat, such as the vernal pools used by spadefoot toads (Scaphiopus couchii) and their parasites (Tinsley and Jackson 1988), could also be uniquely suited for investigation as either soft or hard edges. Additionally, comparing functional traits of parasites in different parts of the host's species range, such as between soft edges in the center and hard edges in the periphery, or comparing parasite characteristics from ecotone specialist host species versus transient host species could provide key information about the selective pressures present in each type of transitional zone (e.g., Kelehear et al. 2012;LaRue et al. 2018;Mayer et al. 2021). We hope that our work here provides a unified conceptual framework and a common terminology that can promote discussion and stimulate further empirical research into host-parasite relationships within edges and transitional zones. ...
Transitional zones, such as edge habitat, are key landscapes for investigating biodiversity. “Soft edges” are permeable corridors that hosts can cross, while “hard edges” are impermeable borders that hosts cannot pass. Although pathogen transmission in the context of edges is vital to species conservation, drivers of host-parasite relationships in ecological edges remain poorly understood. Thus, we defined a framework for testing hypotheses of host-parasite interactions in hard and soft edges by (1) characterizing hard and soft edges from both the host and parasite perspectives, (2) predicting the types of parasites that would be successful in each type of edge, and (3) applying our framework to species invasion fronts as an example of host-parasite relationships in a soft edge. Generally, we posited that parasites in soft edges are more likely to be negatively affected by habitat fragmentation than their hosts because they occupy higher trophic levels but parasite transmission would benefit from increased host connectivity. Parasites along hard edges, however, are at higher risk of local extinction due to host population perturbations with limited opportunity for parasite recolonization. We then used these characteristics to predict functional traits that would lead to parasite success along soft and hard edges. Finally, we applied our framework to invasive species fronts to highlight predictions regarding host connectivity and parasite traits in soft edges. We anticipate that our work will promote a more complete discussion of habitat connectivity using a common framework and stimulate empirical research into host-parasite relationships within ecological edges and transitional zones.
... This result is not necessarily unexpected as the pathogens here examined are often considered specific to the Bombus genus. However, as intestinal parasites represent only a fraction of the potential pathogens transmitted (i.e., viruses should also be considered), we cannot rule out completely the idea of parasite transmission from one species to another, especially considering that susceptibility to new parasites is high in novel hosts [27], and new parasites often experience drastic changes in life history traits that permit them to infect novel hosts [28]. While the co-invasion of B. terrestris and X. augusti to Chile has created a new zone of geographical sympatry for the two otherwise allopatric species, the consequence of their coexistence for disease spread is unknown. ...
Bombus terrestris is a European bumblebee extensively commercialized worldwide for crop pollination. In Chile, this species was introduced in 1997 and after confinement escape, it has spread and established in several localities of central-southern Chile and in the Argentine Patagonia. The South American carpenter bee Xylocopa augusti , in turn, has been recently reported in central Chile, and as B. terrestris , this species has become increasingly common, often found in sympatry with B. terrestris in some localities. While intestinal parasites such as the flagellate trypanosome Crithidia bombi , the microsporidium Nosema bombi , and the neogregarine protozoan Apicystis bombi , show high levels of specialization on the Bombus genus, parasites often increase their host range, especially after invading novel habitats, hence creating new infection disease scenarios. In this work, we used molecular techniques to detect the presence of the intestinal pathogens of B. terrestris in coexisting X. augusti from different localities in the Metropolitan Region of Chile. Our results revealed the presence of the three pathogens in B. terrestris only, with population prevalence broadly similar to that reported in other studies. The carpenter bee X. augusti did not show evidence of any of the three parasites examined, indicating that this invader species is not recipient of any of the parasite species present in B. terrestris .
... The distribution of dace provides the opportunity to compare the population biology of a native helminth species, P. tereticollis, in a native and an invasive species at the core and edge of its range and to investigate the effect of long-established and recently established invasive host populations on parasite dynamics in native brown trout. Following conceptual and empirical studies that suggest that parameters of parasite infection will be lower in an invasive species at the invasion edge (Kelehear et al. 2012;White and Perkins 2012), we hypothesise that dace will be less infected at the edge of their invasive range in the River Barrow. Survey and experimental data from Great Britain indicate that dace become infected with P. laevis s.l. at similar rates to brown trout and host competency for P. laevis s.l. is low but similar for both fish species (Hine and Kennedy 1974a, b). ...
Invasive species tend to acquire native parasites from their invaded range over time. In these cases, native host-parasite dynamics may be altered as a result of differences in parasite population biology and host competency between invasive and native hosts. Competent invasive hosts are likely to increase transmission to native hosts while incompetent invasive hosts may dilute infection in natives. In this study, we used a freshwater fish system and a survey approach to compare the host competency and population biology of a dominant helminth parasite, Pomphorhynchus tereticollis, between native brown trout (Salmo trutta) hosts and invasive dace (Leuciscus leuciscus) hosts over 2 years at the core and edge of dace’s invasive range in Ireland. Our results show that, although dace acquired P. tereticollis, dace had prevalent and high intensity infections of immature extra-intestinal worms while prevalence of adult worms was consistently higher in brown trout. The majority of parasite individuals infecting dace were immature extra-intestinal forms and, in contrast to brown trout, parasites in dace did not attain sexual maturity. In addition, brown trout from the invasion core where dace have been established the longest had a lower abundance of P. tereticollis, indicating that by taking up but not transmitting infective stages of the parasite, invasive dace may dilute P. tereticollis infection in the native host.
Graphic abstract
... A common-garden experiment demonstrated that populations of R. pseudosphaerocephala from the expanding range edge exhibited reduced age at maturity and larger sizes of eggs, infective larvae and free-living adults, when compared to populations from the distribution core. Low host density at the expanding front selected for symbiont traits that enhanced transmission opportunities, thereby favouring symbiont range expansion (Kelehear, Brown & Shine, 2012). In addition, changes in host behaviour such Fig. 4. Hypothetical spatiotemporal relationships among types of biotope colonisation involved in symbiont invasion processes, considering both hosts and land patches inhabited by host communities as biotopes. ...
Range expansion results from complex eco-evolutionary processes where range dynamics and niche shifts interact in a novel physical space and/or environment, with scale playing a major role. Obligate symbionts (i.e. organisms permanently living on hosts) differ from free-living organisms in that they depend on strong biotic interactions with their hosts which alter their niche and spatial dynamics. A symbiotic lifestyle modifies organism-environment relationships across levels of organisation, from individuals to geographical ranges. These changes influence how symbionts experience colonisation and, by extension, range expansion. Here, we investigate the potential implications of a symbiotic lifestyle on range expansion capacity. We present a unified conceptual overview on range expansion of symbionts that integrates concepts grounded in niche and metapopulation theories. Overall, we explain how niche-driven and dispersal-driven processes govern symbiont range dynamics through their interaction across scales, from host switching to geographical range shifts. First, we describe a background framework for range dynamics based on metapopulation concepts applied to symbiont organisation levels. Then, we integrate metapopulation processes operating in the physical space with niche dynamics grounded in the environmental arena. For this purpose, we provide a definition of the biotope (i.e. living place) specific to symbionts as a hinge concept to link the physical and environmental spaces, wherein the biotope unit is a metapopulation patch (either a host individual or a land fragment). Further, we highlight the dual nature of the symbionts' niche, which is characterised by both host traits and the external environment, and define proper conceptual variants to provide a meaningful unification of niche, biotope and symbiont organisation levels. We also explore variation across systems in the relative relevance of both external environment and host traits to the symbiont's niche and their potential implications on range expansion. We describe in detail the potential mechanisms by which hosts, through their function as biotopes, could influence how some symbionts expand their range - depending on the life history and traits of both associates. From the spatial point of view, hosts can extend symbiont dispersal range via host-mediated dispersal, although the requirement for among-host dispersal can challenge symbiont range expansion. From the niche point of view, homeostatic properties of host bodies may allow symbiont populations to become insensitive to off-host environmental gradients during host-mediated dispersal. These two potential benefits of the symbiont-host interaction can enhance symbiont range expansion capacity. On the other hand, the central role of hosts governing the symbiont niche makes symbionts strongly dependent on the availability of suitable hosts. Thus, environmental, dispersal and biotic barriers faced by suitable hosts apply also to the symbiont, unless eventual opportunities for host switching allow the symbiont to expand its repertoire of suitable hosts (thus expanding its fundamental niche). Finally, symbionts can also improve their range expansion capacity through their impacts on hosts, via protecting their affiliated hosts from environmental harshness through biotic facilitation.
... Higher gonadosomatic index at population edges has been documented in sea urchins [18] and fishes [19][20][21]. Other adaptations can also contribute to higher reproductive success for "edge" populations, such as increased metabolic rate allowing more time for oviposition [22], larger body size facilitating higher fecundity [23][24][25], and larger or more rapidly-growing offspring [26][27][28][29]. Fishes with highly successful reproduction in a wide range of contexts are more likely to become a successful invasive species than fishes with very specific requirements for reproduction [30,31]. ...
Reproduction is a major component of an animal’s life history strategy. Species with plasticity in their reproductive biology are likely to be successful as an invasive species, as they can adapt their reproductive effort during various phases of a biological invasion. Silver carp (Hypophthalmicthys molitrix), an invasive cyprinid in North America, display wide variation in reproductive strategies across both their native and introduced ranges, though the specifics of silver carp reproduction in the Illinois River have not been established. We assessed reproductive status using histological and endocrinological methods in silver carp between April–October 2018, with additional histological data from August–October 2017. Here we show that female silver carp are batch spawners with asynchronous, indeterminate oocyte recruitment, while male silver carp utilize a determinate pattern of spermatogenesis which ceases in the early summer. High plasma testosterone levels in females could be responsible for regulating oocyte development. Our results suggest that silver carp have high spawning activity in the early summer (May–June), but outside of the peak spawning period, female silver carp can maintain spawning-capable status by adjusting rates of gametogenesis and atresia in response to environmental conditions, while males regress their gonads as early as July. The results of this study are compared to reports of silver carp reproduction in other North American rivers as well as in Asia.
... The resulting distribution of host demographic phases enables pathogens to potentially diversify along a colonizer-competitor axis (Wei and Krone 2005;de Roode et al. 2008;Magalon et al. 2010), such that pathogens that excel at establishing in newly colonized host populations are likely to be less fit in host populations at overshoot or carrying capacity. If such a diversification and trade-off exist, it has important implications for emerging theory on the evolution of virulence during invasions (Griette et al. 2015;Osnas et al. 2015;Lion and Gandon 2016), but it has rarely (if ever) been demonstrated empirically (but see Kelehear et al. 2012;Phillips et al. 2012;Mondet et al. 2014). By experimentally introducing pathogens into experimental host populations undergoing different phases of colonization, we show that the conditions required for diversifying selection for a pathogen is indeed embedded within the demography of the host population. ...
Repeated extinction and recolonization events generate a landscape of host populations that vary in their time since colonization. Within this dynamic landscape, pathogens that excel at invading recently colonized host populations are not necessarily those that perform best in host populations at or near their carrying capacity, potentially giving rise to divergent selection for pathogen traits that mediate the invasion process. Rarely, however, has this contention been empirically tested. Using Daphnia magna, we explored how differences in the colonization history of a host population influence the invasion success of different genotypes of the pathogen Pasteuria ramosa. By partitioning the pathogen invasion process into a series of individual steps, we show that each pathogen optimizes invasion differently when encountering host populations that vary in their time since colonization. All pathogen genotypes were more likely to establish successfully in recently colonized host populations, but the production of transmission spores was typically maximized in either the subsequent growth or stationary phase of host colonization. Integrating across the first three pathogen invasion steps (initial establishment, proliferation, and secondary infection) revealed that overall pathogen invasion success (and its variance) was, nonetheless, highest in recently colonized host populations. However, only pathogens that were slow to kill their host were able to maximize host‐facilitated dispersal. This suggests that only a subset of pathogen genotypes—the less virulent and more dispersive—are more likely to encounter newly colonized host populations at the front of a range expansion or in metapopulations with high extinction rates. Our results suggest a fundamental trade‐off for a pathogen between dispersal and virulence, and evidence for higher invasion success in younger host populations, a finding with clear implications for pathogen evolution in spatiotemporally dynamic settings.
... Given the low prevalence of the parasite in its native range, both in our study and in every prior study of which we are aware (Figures 1 and 2), it seems unlikely that our coevolved popula- We note also that our work examines only half of the potential coevolutionary story. While we focus here on host evolution in response to parasitism, it is likely that the parasite is also evolving as it expands into new host populations (Kelehear, Brown, & Shine, 2012). Interestingly, our findings of increased susceptibility in novel host populations contrasts with work done in a snail host-trematode parasite system supporting the matching alleles hypothesis, in which hosts are more susceptible to coevolved parasite populations (King, Delph, Jokela, & Lively, 2009). ...
Parasitism can represent a potent agent of selection, and introduced parasites have the potential to substantially alter their new hosts' ecology and evolution. While significant impacts have been reported for parasites that switch to new host species, the effects of macroparasite introduction into naïve populations of host species with which they have evolved remains poorly understood. Here, we investigate how the estuarine white‐fingered mud crab (Rhithropanopeus harrisii) has adapted to parasitism by an introduced rhizocephalan parasite (Loxothylacus panopaei) that castrates its host. While the host crab is native to much of the East and Gulf Coasts of North America, its parasite is native only to the southern end of this range. Fifty years ago, the parasite invaded the mid‐Atlantic, gradually expanding through previously naïve host populations. Thus, different populations of the same host species have experienced different degrees of historical interaction (and thus potential evolutionary response time) with the parasite: long‐term, short‐term, and naïve. In nine estuaries across this range, we examined if and how parasite prevalence and host susceptibility to parasitism differs depending on the length of the host's history with the parasite. In field surveys, we found that the parasite was significantly more prevalent in its introduced range (i.e., short‐term interaction) than in its native range (long‐term interaction), a result that was also supported by a meta‐analysis of prevalence data covering the 50 years since its introduction. In controlled laboratory experiments, host susceptibility to parasitism was significantly higher in naïve hosts than in hosts from the parasite's native range, suggesting that host resistance to parasitism is under selection. These results suggest that differences in host‐parasite historical interaction can alter the consequences of parasite introductions in host populations. As anthropogenically‐driven range shifts continue, disruptions of host‐parasite evolutionary relationships may become an increasingly important driver of ecological and evolutionary change. This article is protected by copyright. All rights reserved.
... Life history traits are generally regarded as evolutionary versatile as rapid adaptive responses of such traits to local selection pressures have been demonstrated for a variety of organisms (Jensen et al., 2008;Kelehear, Brown, & Shine, 2012). However, with a design based on genotypes from multiple population origins, our study observed robust differences between species. ...
(1) Brachionus calyciflorus is arguably the most studied freshwater monogonont rotifer. Although it has been recognized as a cryptic species complex for more than a decade, a formal (re-)description of the four species known so far (B. calyciflorus, B. dorcas, B. elevatus and B. fernandoi) has only recently been made. Information on the ecology of these species is very scant and fragmented. The aim of this study was to test for ecological divergence between these four species, specifically their life history strategy and population demography.
(2) We conducted a life history experiment using 12-16 genotypes per species. For each species, genotypes were extracted from at least three different natural populations. In addition, we performed population-level culture experiments with the aim to compare population growth rates and demographic structure of experimental populations among species. Finally, we searched the literature for life history studies with molecular data allowing retrospective species identification.
(3) We found pronounced differences in life history traits between B. fernandoi and the other three species. B. fernandoi had higher egg and juvenile development times and a lower egg production rate and mictic ratio. We detected no significant life history differences among B. calyciflorus, B. elevatus and B. dorcas.
(4) Population growth rates of B. fernandoi and B. calyciflorus were higher than those of B. elevatus and B. dorcas. Life history divergence resulted in marked differences in the demographic structure of populations. Populations of B. fernandoi contained larger fractions of pre-reproductive females and lower fractions of adult females with sexual eggs than populations of B. calyciflorus, B. elevatus and B. dorcas. Mortality was found to be highest in B. elevatus and lowest in B. calyciflorus populations.
(5) Our results show that a reverse taxonomy approach is powerful in revealing sources of variation in ecologically relevant traits of cryptic species, such as life history and demographic structure. Explicit consideration of this variation is crucial for future studies of their dynamics in natural communities.
... It would be particularly interesting to confirm this trend in a common garden experiments. Such an experiment was carried out to monitor the evolution of the nematode lungworm (Rhabdias marina), a parasite of the invasive cane toads (Rhinella marina) in Australia [135]. Nematodes from the edge of the invasion exhibited very distinct life history traits (larger eggs, larger free-living larvae, larger infective larvae and reduced age at maturity). ...
In this thesis we consider several models of propagation arising in evolutionary epidemiology. We aim at performing a rigorous mathematical analysis leading to new biological insights. At first we investigate the spread of an epidemic in a population of homogeneously distributed hosts on a straight line. An underlying mutation process can shift the virulence of the pathogen between two values, causing an interaction between epidemiology and evolution. We study the propagation speed of the epidemic and the influence of some biologically relevant quantities, like the effects of stochasticity caused by the hosts' finite population size (numerical explorations), on this speed. In a second part we take into account a periodic heterogeneity in the hosts' population and study the propagation speed and the existence of pulsating fronts for the associated (non-cooperative) reaction-diffusion system. Finally, we consider a model in which the pathogen is allowed to shift between a large number of different phenotypes, and construct possibly singular traveling waves for the associated nonlocal equation, thus modelling concentration on an optimal trait.
... After the toad defecates, these free-living larvae mate to produce infective third-stage larvae (L3) that develop inside their mother for up to 4 days before breaking free and entering the soil (Baker, 1979). When an L3 locates an anuran host, it pierces through the epidermis and migrates through tissue to reach the lungs of the toad where it feeds on blood from capillary beds (Pizzatto, Shilton, & Shine, 2010) and can mature in as few as 5 days (Kelehear, Brown, & Shine, 2012). Although infection dynamics vary seasonally and climatically (Barton, 1998;Pizzatto et al., 2013), the parasite is common in some populations of toads in Australia (>80% of toads infected: Barton, 1998), with up to 282 adult worms per host (Pizzatto et al., 2013). ...
Parasites can enhance their fitness by modifying the behavior of their hosts in ways that increase rates of production and transmission of parasite larvae. We used an antihelminthic drug to experimentally alter infections of lungworms (Rhabdias pseudosphaerocephala) in cane toads (Rhinella marina). We then compared subsequent behaviors of dewormed toads versus toads that retained infections. Both in the laboratory and in the field, the presence of parasites induced hosts to select higher body temperatures (thereby increasing rates of lungworm egg production), to defecate in moister sites, and to produce feces with higher moisture content (thereby enhancing survival of larvae shed in feces). Because those behavioral modifications enhance rather than decrease parasite fitness, they are likely to have arisen as adaptive manipulations of host behavior rather than as host adaptations to combat infection or as nonadaptive consequences of infection on host physiology. However, the mechanisms by which lungworms alter cane toad thermal preference and defecation are not known. Although many examples of host manipulation by parasites involve intermediate hosts facilitating their own demise, our findings indicate that manipulation of definitive hosts can be as subtle as when and where to defecate.
... In this approach, hosts and parasites are taken from several locations along their invasion route for controlled cross infection experiments. This setup can help elucidate how the duration of co-evolution influences the evolution of the host resistance and tolerance, as well as the parasite's infectivity and virulence in the wild ( Feis et al. 2016;Kelehear et al. 2012;Weclawski et al. 2013), without the need to raise multiple generations in the lab to use in time-shift experiments (i.e. in Brockhurst et al. 2007;Schulte et al. 2010). Unlike time-shift experiments, however, hosts at invasion fronts are at the start of their co-evolutionary interaction, whereas parasites have been moving across the host population for some time near the invasion origin. ...
On theoretical grounds, antagonistic co-evolution between hosts and their parasites should be a widespread phenomenon but only received little empirical support so far. Consequently, the underlying molecular mechanisms and evolutionary steps remain elusive, especially in non-model systems. Here, we utilised the natural history of invasive parasites to document the molecular underpinnings of co-evolutionary trajectories. We applied a dual-species transcriptomics approach to experimental cross-infections of blue mussel Mytilus edulis hosts and their invasive parasitic copepods Mytilicola intestinalis from two invasion fronts in the Wadden Sea. We identified differentially regulated genes from an experimental infection contrast for hosts (infected versus control) and a sympatry contrast (sympatric versus allopatric combinations) for both hosts and parasites. The damage incurred by Mytilicola infection and the following immune response of the host was mainly reflected in cell division processes, wound healing, apoptosis and the production of reactive oxygen species (ROS). Furthermore, the functional coupling of host and parasite sympatry contrasts revealed the concerted regulation of chitin digestion by a Chitotriosidase1 homolog in hosts with several cuticle proteins in the parasite. Together with the coupled regulation of ROS producers and antagonists, these genes represent candidates that mediate the different evolutionary trajectories within the parasite's invasion. The host-parasite combination-specific coupling of these effector mechanisms suggests that underlying recognition mechanisms create specificity and local adaptation. In this way, our study demonstrates the use of invasive species’ natural history to elucidate molecular mechanisms of host-parasite co-evolution in the wild. This article is protected by copyright. All rights reserved.
... A potential factor affecting the acquisition of enemies is associated with the location of populations within the introduced range. A species' abundance is generally greater at the centre of its range and decreases towards the range edges, either as a result of declining habitat quality (abundant centre model, Angert and Schemske 2005;Vaupel and Matthies 2012) or as a product of range expansion as species gradually disperse from their point of establishment/introduction (Fagan and Bishop 2000;Tsai and Manos 2010;Kelehear et al. 2012). This greater Communicated by Wayne Dawson. ...
Release from natural enemies is often cited as a key factor for understanding the success of invasive plant species in novel environments. However, with time invasive species will accumulate native enemies in their invaded range, with factors such as spread distance from the site of introduction, climate and leaf-level traits potentially affecting enemy acquisition rates. However, the influence of such factors is difficult to assess without examining enemy attack across the entire species’ range. We tested the significance of factors associated with range expansion (distance from source population and maximum population density), climatic variables (annual temperature and rainfall) and leaf-level traits [specific leaf area (SLA) and foliar nitrogen concentration] in explaining variation in enemy damage across multiple populations of two coastal invasive plants (Gladiolus gueinzii Kunze and Hydrocotyle bonariensis Lam.) along their entire introduced distribution in eastern Australia. We found that for H. bonariensis, amount of foliar damage increased with distance from source population. In contrast, for G. gueinzii, probability and amount of foliar damage decreased with decreasing temperature and increasing rainfall, respectively. Our results show that patterns of enemy attack across species’ ranges are complex and cannot be generalised between species or even range edges.
... Individuals at the expanding range edge experience different demographic, physiological and environmental pressures than those faced by conspecifics from the range core, often leading to phenotypic divergence across the invasion range [1]. For example, vanguard individuals often have distinctive phenotypes associated with faster dispersal such as larger size [2][3][4], longer legs [5] and increased investment in dispersal appendages and mass in plant seeds [6][7][8]. More generally, successful invaders exhibit a suite of physiological, lifehistory, morphological and behavioural traits that enhance dispersal rates and facilitate functioning in novel environments (known as an 'Invasion Syndrome'; [9,10]). ...
Individuals at the leading edge of expanding biological invasions often show distinctive phenotypic traits, in ways that enhance their ability to disperse rapidly and to function effectively in novel environments. Cane toads (Rhinella marina) at the invasion front in Australia exhibit shifts in morphology, physiology and behaviour (directionality of dispersal, boldness, risk-taking). We took a common-garden approach, raising toads from range-core and range-edge populations in captivity, to see if the behavioural divergences observed in wild-caught toads are also evident in common-garden offspring. Captive-raised toads from the invasion vanguard population were more exploratory and bolder (more prone to ‘risky’ behaviours) than toads from the range core, which suggests that these are evolved, genetic traits. Our study highlights the importance of behaviour as being potentially adaptive in invasive populations and adds these behavioural traits to the increasing list of phenotypic traits that have evolved rapidly during the toads’ 80-year spread through tropical Australia.
... Une explication alternative pourrait aussi être en rapport avec l'évolution de la virulence de certains parasites conservés au cours de l'invasion, soit du fait de la modification de l'infracommunauté de parasites, soit par un mécanisme de sélection. Une récente étude a ainsi montré une évolution rapide des traits d'histoire de vie (plus grande taille des oeufs et des stades de développement, maturité atteinte rapidement) des nématodes de la grenouille Rhinella marina envahissante en Australie sous l'effet de pressions sélectives inhérentes à l'expansion en cours de leur hôte (Kelehear et al., 2012 ...
Les invasions biologiques sont de plus en plus fréquentes, avec des conséquences importantes sur la biodiversité et la santé humaine. Étudier les mécanismes qui les expliquent permet simultanément (i) d’envisager des stratégies efficaces de contrôle et de prévention et (ii) d’étudier divers processus écologiques et évolutifs sur des échelles de temps contemporaines. Plusieurs hypothèses basées sur le parasitisme et l’immunité des hôtes sont proposées pour expliquer le succès des espèces envahissantes. Ainsi, au cours de l’invasion, les hôtes exotiques (1) perdraient leurs parasites naturels (Enemy Release, ER), (2) transfèreraient leurs parasites exotiques aux hôtes natifs (Spill-Over, SO) et/ou (3) amplifieraient les cycles des parasites natifs au sein des hôtes locaux (Spill-Back, SB). En relation avec ces changements dans les interactions hôtes-parasites, l’hypothèse EICA (Evolution of Increased Competitive Ability) prédit une modulation des ressources de l’hôte envahissant via un investissement moins important dans les réponses immunitaires coûteuses (inflammation) au profit de réponses immunitaires beaucoup moins coûteuses (réponses médiées par les anticorps) et de capacités de reproduction et de dispersion des populations sur le front d’invasion. Le but de ma thèse est de tester ces prédictions dans le cadre de deux invasions actuellement en cours au Sénégal : celles du rat noir Rattus rattus et de la souris domestique Mus musculus domesticus, deux espèces envahissantes majeures tant par leurs impacts (économique, sanitaire, écologique) que par leur distribution quasiment mondiale. Mes travaux se basent sur un dispositif d’échantillonnage en populations naturelles et sur le développement d’approches comparatives le long d’un gradient d’invasion pour chacune des deux espèces exotiques. Les patrons de structure (prévalence, abondance, richesse) de deux communautés de parasites (helminthes gastro-intestinaux, bactéries pathogènes) et les profils immunitaires (réponses médiées par les anticorps naturels, inflammation) des rongeurs commensaux exotiques (M. m. domesticus, R. rattus) et/ou natifs (Mastomys spp.) ont été comparés pour des localités situées dans des régions anciennement envahies (depuis plus de 100 ans), récemment envahies (depuis moins de 30 an : front d’invasion), et non envahies. Mes résultats montrent des variations dans la structure des communautés de parasites et les réponses immunitaires des hôtes natifs et exotiques. Les tendances observées, aussi bien pour les communautés de parasites que pour les composantes immunitaires étudiées le long des deux routes d’invasion, attestent de patrons globalement plus complexes qu’attendu sous les hypothèses de départ, suggérant l’existence de relations complexes entre caractéristiques des communautés d’hôtes et de parasites, investissement immunitaire, conditions environnementales et invasions biologiques. Des approches expérimentales doivent être envisagées afin de déterminer les conséquences et les mécanismes sous-jacents aux différents phénomènes observés.
... When an L3 locates an anuran host it pierces through the skin, alimentary tract or membrane behind the eye and burrows through tissue to reach the lungs of the toad where it feeds on blood (Pizzatto et al., 2010). After they reach the host's lungs the parasites mature and begin producing eggs in as little as 5 days (Kelehear et al., 2012). Although infection dynamics can vary climatically and seasonally (Barton, 1998;Pizzatto et al., 2013), up to 80% of cane toads are infected in populations in far north Queensland (Barton, 1998), with infection intensity reaching up to 282 adult worms per host (Pizzatto et al., 2013). ...
The immunological and pathological consequences of parasite infection can be more rigorously assessed from experimental manipulation than from correlational studies of natural infections. We used anthelmintic treatment to experimentally decrease intensities of lungworm infection in captive and free-ranging wild cane toads to assess parasite impacts on host immune responses. First, we administered the anthelmintic drug Ivermectin to both infected and uninfected toads, to distinguish drug effects per se from the impacts of killing lungworms. Worms began dying and decomposing <48 h after injection. The only immunological variables that were affected by anthelmintic treatment were bactericidal capacity of the blood which increased in parasitized toads (presumably triggered by decomposing worms in the lungs), and the phagocytic capacity of blood (which increased in both infected and uninfected toads); the latter effect presumably was caused by the injection of Ivermectin per se rather than removal of parasites. Second, we looked at correlates of variation in the infection intensity induced by de-worming (in both captive and free-ranging toads) over an eight-week period. Heavier lungworm infection was associated with increased phagocytic ability of the host's blood, and a reduction in the host's liver mass (and hence, energy stores). Experimental de-worming thus revealed pathological and immunological costs of the presence of lungworms, and of their removal by anthelmintic injection.
... Heightened virulence of white-tailed deer parasites could facilitate this range expansion through reduced competition with sympatric moose and elk, and benefit both deer and their parasites (Schmitz and Nudds 1994). Selection for virulence may also happen rapidly, as rapid evolution has been identified in other parasites expanding along range edges (Kelehear et al. 2012). ...
The giant liver fluke, Fascioloides magna, is a possible contributing factor to moose
(Alces alces) declines in North America, but evidence linking F. magna infection directly to moose
mortality is scarce. This review identifies knowledge gaps about the transmission and impact of
F. magna infection on moose and proposes new directions for research and management of this parasite. We suggest that the importance of intermediate snail hosts has been largely neglected in current
management discussions and warrants greater emphasis. The intermediate hosts responsible for
F. magna transmission likely vary by region and recent genetic evidence suggests that F. magna was
restricted to several isolated refugia during cervid extirpation events in North America. This distributional history represents several coevolutionary and pathological implications for definitive hosts
of F. magna. We suggest that F. magna infections are most ecologically significant as they relate to
sublethal impacts and multiple parasitic infections. In assessing infection risk on landscapes, most
models rely heavily on monitoring white-tailed deer (Odocoileus virginianus), but this approach
only measures risk indirectly. The reliability and accuracy of models would probably improve if snail
habitat in ephemeral wetlands was included as a predictor variable.
... Eggs are then swallowed into the digestive system, and passed into the environment 199 through host faeces ). Newly hatched larvae escape from faeces into the soil, where 200 they moult several times and develop into free-living sexually reproducing adults (Baker 1979, 201 Anderson 2000) over the span of 24-48 hours (Kelehear et al. 2012a). Offspring develop within the 202 free-living mother and eventually consume her (4-10 days after toad defecation: Kelehear et al. 2012a), 203 and enter the environment as infective third-stage larvae (L3) (Baker 1979, Anderson 2000. ...
Brought to Australia in 1935 to control agricultural pests (from French Guiana, via Martinique, Barbados, Jamaica, Puerto Rico and Hawai'i), repeated stepwise translocations of small numbers of founders enabled the cane toad (Rhinella marina) to escape many parasites and pathogens from its native range. However, the infective organisms that survived the journey continue to affect the dynamics of the toad in its new environment. In Australia, the native-range lungworm Rhabdias pseudosphaerocephala decreases its host's cardiac capacity, as well as growth and survival, but not rate of dispersal. The lungworm is most prevalent in long-colonised areas within the toads' Australian range, and absent from the invasion front. Several parasites and pathogens of Australian taxa have host-shifted to cane toads in Australia; for example, invasion-front toads are susceptible to spinal arthritis caused by the soil bacterium, Ochrobactrum anthropi. The pentastome Raillietiella frenata has host-shifted to toads and may thereby expand its Australian range due to the continued range expansion of the invasive toads. Spill-over and spill-back of parasites may be detrimental to other host species; however, toads may also reduce parasite loads in native taxa by acting as terminal hosts. We review the impact of the toad's parasites and pathogens on the invasive anuran's biology in Australia, as well as collateral effects of toad-borne parasites and pathogens on other host species in Australia. Both novel and co-evolved pathogens and parasites may have played significant roles in shaping the rapid evolution of immune system responses in cane toads within their invaded range.
... Current Zoology Vol. 60 No. 4 evolving under increasing levels of virulence. Rapid evolution of parasite life history traits has been observed in other systems Jones et al. 2008;Kelehear et al., 2012) and requires further study in this system. Theory predicts that parasites should become locally adapted -that is, have a fitness advantage in sympatric hosts over allopatric hosts that cannot be invaded by other non-adapted parasites . ...
The significance of hybridisation for biodiversity has been the subject of a long-standing debate. Hybridisation has been characterised as being detrimental for biodiversity and speciation as it can blur the borders between distinct species. Contrastingly, hybridisation has also been described as a creative evolutionary process generating increased genetic variation and facilitating adaptation. Only few study systems enable us to observe hybridisation in real time, which has limited our knowledge of its consequences for the ecology and conservation management of contemporary species. This study investigates current hybridisation between two species of Darwin’s finches (small tree finch Camarhynchus parvulus and medium tree finch C. pauper) on Floreana Island, Galápagos, Ecuador, and tests key variables related to foraging ecology, song, gene flow, and parasitism in hybrids and their two parental species.
The current ecological positions of hybrids in relation to parental species are important to identify possible selection pressures that could favour different phenotypes across vertical or horizontal clines. I examined foraging behaviour in relation to vertical habitat use in Darwin’s tree finches and hybrid birds as the proportion of hybrids increased across the decade. Both parental species changed foraging height or behaviour with increasing hybrid density, while hybrid foraging behaviour was consistent across years. These findings suggest that parental species and hybrids may be experiencing different selection pressures, and the increasing hybrid abundance could be influencing the foraging behaviour of their parental species. Given the importance of rapid assessment for regular biodiversity monitoring, I investigated if hybrid birds could be acoustically identified, by comparing their song with song of the two parental species. While C. pauper had a distinct song, hybrid birds and C. parvulus song was indistinguishable and their respective populations could therefore not be surveyed individually. Acoustical surveys across the decade 2004–2013 showed 52 % decline of the critically endangered C. pauper, highlighting the need for targeted conservation actions. Next, I examined the role of female choice as a driver of the hybridisation using a powerful combination of pairing observations and genetic analysis with nine microsatellite markers. I found that C. pauper females did not discriminate heterospecifics and frequently paired with C. parvulus males, while C. parvulus females were never observed to pair with C. pauper males. Hybrid females paired predominantly with hybrid and C. parvulus males, resulting in asymmetrical introgression with gene flow skewed towards C. parvulus. These findings support the formation of a hybrid swarm comprising C. parvulus and hybrids of various generations while C. pauper retains most of its genetic purity.
Reproductive success is a key measure of biological fitness. I analysed nesting success in Camarhynchus and Geospiza fuliginosa and identified parasite intensity due to larvae of the introduced fly Philornis downsi, whose parasitic larvae have been identified as the primary cause ofnestling mortality. Hybrid birds had lowest in-nest P. downsi numbers, providing the first evidence of hybrid fitness in this system.
This thesis uses a combination of behavioural, genetic and monitoring methods to assess the survival of hybrids in a rapidly evolving vertebrate system. Under conditions of extreme natural selection from the recently introduced fly P. downsi, hybrid fitness was higher than that of the parental species as measured by fewer parasites per nests. I have identified the role of sexual selection in forming the hybrids via female choice of heterospecific males, and the role of natural selection in maintaining the hybrid offspring, It is my hope that the findings of this thesis will encourage conservation efforts of the Darwin’s finch species complex including the hybrid birds.
... In particular, these models highlight the build-up of phenotypic variation between the front and the rear of a spreading epidemic. In accord with these theoretical results, recent field studies report the existence of patterns of phenotypic differentiation between pathogens sampled at the front or at the epicentre of epidemics [19,[23][24][25]. ...
Most spatial models of host-parasite interactions either neglect the possibility of pathogen evolution or consider that this process is slow enough for epidemiological dynamics to reach an equilibrium on a fast timescale. Here, we propose a novel approach to jointly model the epidemiological and evolutionary dynamics of spatially structured host and pathogen populations. Starting from a multi-strain epidemiological model, we use a combination of spatial moment equations and quantitative genetics to analyse the dynamics of mean transmission and virulence in the population. A key insight of our approach is that, even in the absence of long-term evolutionary consequences, spatial structure can affect the short-term evolution of pathogens because of the build-up of spatial differentiation in mean virulence.We show that spatial differentiation is driven by a balance between epidemiological and genetic effects, and this quantity is related to the effect of kin competition discussed in previous studies of parasite evolution in spatially structured host populations. Our analysis can be used to understand and predict the transient evolutionary dynamics of pathogens and the emergence of spatial patterns of phenotypic variation. © 2016 The Author(s) Published by the Royal Society. All rights reserved.
... First, the parasite is readily transmitted to a native frog species (Litoria splendida), where it causes high mortality (Pizzatto & Shine, 2012). Second, low host densities at the toad invasion front reduce parasite transmission rates, so that the lungworms would be unlikely to flourish (Kelehear et al., 2012b). To overcome the latter problem, we could provide additional hosts by experimentally infecting a "Typhoid Mary" species of native frog, Litoria caerulea, that can carry the parasite but is not harmed by it (Pizzatto & Shine, 2011. ...
Parasites may suppress the immune function of infected hosts using microRNAs (miRNAs) to prevent protein production. Nonetheless, little is known about the diversity of miRNAs and their mode(s) of action. In this study, we investigated the effects of infection by a parasitic lungworm ( Rhabdias pseudosphaerocephala ) on miRNA and mRNA expression of its host, the invasive cane toad ( Rhinella marina ). To investigate the cane toad's innate and adaptive immune response to this parasite, we compared miRNA and mRNA expression in naïve toads that had never been infected by lungworms to toads that were infected with lungworms for the first time in their lives, and toads that were infected the second time in their lives (i.e., had two consecutive infections). In total, we identified 101 known miRNAs and 86 potential novel miRNAs. Compared to uninfected and single‐infection toads, multiple‐infection animals drastically downregulated three miRNAs. These miRNAs were associated with gene pathways related to the immune response, potentially reflecting the immunosuppression of cane toads by their parasites . Infected hosts did not respond with substantially differential mRNA transcription; only one gene was differentially expressed between control and single‐infection hosts. Our study suggests that miRNA may play an important role in mediating host–parasite interactions in a system in which an ongoing range expansion by the host has generated substantial divergence in host–parasite interactions.
Dispersal evolution modifies diverse spatial processes, such as range expansions or biological invasions of single species, but we are currently lacking a realistic vision for metacommunities. Focusing on antagonistic species interactions, we review existing theory of dispersal evolution between natural enemies, and explain how this might be relevant for classic themes in host-parasite evolutionary ecology, namely virulence evolution or local adaptation. Specifically, we highlight the importance of considering the simultaneous (co)evolution of dispersal and interaction traits. Linking such multi-trait evolution with reciprocal demographic and epidemiological feedbacks might change basic predictions about coevolutionary processes and spatial dynamics of interacting species. Future challenges concern the integration of system-specific disease ecology or spatial modifiers, such as spatial network structure or environmental heterogeneity.
Parasites may suppress the immune function of an infected host using microRNAs (miRNAs) to prevent protein production. Nonetheless, little is known about the diversity of miRNAs and their mode(s) of action. In this study, we investigated the effects of infection by a parasitic lungworm ( Rhabdias pseudosphaerocephala ) on miRNA and mRNA expression of its host, the invasive cane toad ( Rhinella marina ). We compared miRNA and mRNA expression in naive toads that had never been infected by lungworms to toads that were infected with lungworms for the first time in their lives, and to toads that were infected the second time in their lives (i.e., had two consecutive infections). In total, we identified 434 known miRNAs and 106 potential novel miRNAs. Compared to uninfected toads, infected animals upregulated five (single-infection treatment) or four (multiple-infection treatment) miRNAs. Seven of these differentially expressed miRNAs were associated with gene pathways related to the immune response, potentially reflecting immunosuppression of cane toads by their parasites. Infected hosts did not respond with substantial mRNA transcription, with only one differentially expressed gene between control and single-infection hosts. Our study suggests that miRNA-mediated interactions may play a role in mediating the interaction between the parasite and its host. Our findings clarify the role of miRNAs in host-parasite interactions, in a system in which an ongoing range expansion by the host has generated substantial divergence in host-parasite interactions.
Rhabdias pseudosphaerocephala is a well-studied invasive nematode parasite of amphibians. However, there are several outstanding questions about R. pseudosphaerocephala that are best answered using genomic data. This species differs phenotypically across its invasive range. These differences are challenging to interpret because this species is part of a complex that is diverse and cryptic in its home-range, and we do not know how many species from this complex originally colonised Australia. For this reason, it is unknown whether the phenotypic differences across the introduced range are due to intraspecific differentiation between populations or due to the presence of multiple species. In addition, there is little consensus in the placement of Rhabdiasidae family within the phylum Nematoda, making it difficult to perform comparative analyses with other nematodes. Within this paper, we assemble a reference genome for R. pseudosphaerocephala, the first assembly of any Rhabdiasidae species. We then use resequencing data to address outstanding questions about this species. Specifically, we combine population genetic and phylogenetic analyses to determine that there is likely only a single R. pseudosphaerocephala lineage within Australia, and identify that the invasive range population is closely related to home rage isolates that infect similar host species. We present compelling evidence for a genetic bottleneck following introduction to Australia and genetic differentiation occurring between invasive range populations. We then use genome-scale phylogenomic analysis to place the Rhabdiasidae family in the suborder Rhabditina. Ultimately, this paper brings the study of Rhabdiasidae into the genomic era, and sheds light on its ancient and modern evolutionary history.
Global climate change is now evident across the globe and appears to be accelerating. In Southeast Asia this will lead to substantial increases in temperature and regional changes in rainfall patterns with some areas experiencing wetter conditions and others increased drought. Complicating factors include severe weather events, sea level rise, and drought-induced wild fires. As parasites are reliant on the external environment during parts of their life cycle and are endothermic, such changes will influence both the chances of parasite survival and population dynamics. In addition, hosts will also be influenced by these factors compounding the effects of climate. Our database is still limited and studies of local and regional parasite communities are essential for our understanding of climate impact on human and animal health.
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.
Parasites can alter host and vector phenotype and thereby affect ecological processes in natural populations. Laboratory studies have shown that Borrelia burgdorferi sensu lato, the causative agent of human Lyme borreliosis, induces physiological alterations in its main tick vector in Europe, Ixodes ricinus , which increase its survival under challenging conditions. We hypothesise that these phenotypic alterations may allow I. ricinus to colonise marginal habitats, thereby fuelling the ongoing range expansion of I. ricinus towards higher elevations and latitudes induced by climate change. To explore the potential for such an effect under natural conditions, we studied the prevalence of B. burgdorferi s.l. in questing I. ricinus and its variation with elevation in the Swiss Alps. We screened for B. burgdorferi s.l. infection in questing nymphs of I. ricinus (N = 411) from 15 sites between 528 and 1774 m.a.s.l to test if B. burgdorferi s.l. prevalence is higher at high elevations (i.e. in marginal habitats). We found that B. burgdorferi s.l. prevalence in I. ricinus nymphs decreased linearly with increasing elevation and that it was 12.6% lower in I. ricinus nymphs collected at high elevations compared to nymphs in the core range. Thus, we found no evidence that the B. burgdorferi s.l.-induced alterations of I. ricinus phenotype facilitate the colonisation of marginal habitats in the wild. These findings have implications for a better understanding of eco-evolutionary processes in natural host-parasite systems, as well as the assessment of Lyme borreliosis risk in regions where I. ricinus is newly emerging.
Parasite life history can be affected by conditions of the host and of the external environment. Rapamycin, a known immunosuppressant of mammals, was fed to laboratory mice that were then infected with the Trichostrongylid nematode Heligmosomoides bakeri to determine if host rapamycin exposure would affect parasite survival, growth, and reproduction. In addition, adult worms from control fed mice were directly exposed to rapamycin to assess if rapamycin would affect worm viability and ex vivo reproduction. We found that host ingestion of rapamycin did not affect H. bakeri survival or growth for male or female worms, but female worms had increased reproduction both in vivo and when removed from the host and cultured ex vivo. After direct rapamycin exposure, motility of female worms was greater at low levels of rapamycin compared to high levels of rapamycin or high levels of DMSO (the vehicle used to solubilize rapamycin) in control media, but was similar to females in low levels of DMSO in control media. Male motility was not affected by the presence of rapamycin or DMSO in the media. Ex vivo egg deposition was higher when exposed to rapamycin than when cultured in control media that contained DMSO, regardless of DMSO dose. Overall, we conclude that host ingestion of rapamycin or direct exposure to rapamycin was generally favorable or neutral for parasite life history traits.
Acute activation of the immune system often initiates a suite of behavioural changes. These “sickness behaviours”—involving lethargy and decreased activity—may be particularly costly on invasion fronts, where evolutionary pressures on dispersal favour individuals that move large distances.
We used a combination of field and laboratory studies to compare sickness behaviours of cane toads from populations differing in invasion history. To do this we stimulated immune system activation by injecting lipopolysaccharide ( LPS ) to mimic bacterial infection.
We predicted that LPS would result in less severe sickness behaviour in toads from range‐edge populations because they had undergone selection for rapid and sustained dispersal (activities in conflict with lethargy and decreased activity).
Contrary to our prediction, LPS injection caused a greater reduction in dispersal‐relevant traits in invasion‐front individuals than in conspecifics from the range‐core.
Our data suggest that the rapid invasion of cane toads through tropical Australia has seen an evolutionary shift in the magnitude of sickness behaviour elicited by pathogen infection. The increased sickness behaviour among range‐edge toads suggests a shift away from pathogen tolerance (seen in range‐core populations) towards resistance to pathogen attack. But as a consequence, when pathogens do become successfully established, toads from invasion‐front populations may have less capacity to tolerate their ill‐effects.
Genetic and morphological attributes of modern Pinus contorta spp latifolia (Rocky Mountain subspecies) are related to time since founding. Reduced allelic diversity towards the northern periphery may result simply from the stochastic effects of repeated long-distance founding events during continental-scale, postglacial spread. An increase in the ability of seeds to disperse as migration proceeds may result from directional selection associated with long-distance dispersal events occurring as part of the migration process. The magnitude of differences between central and marginal populations would be smaller because gene flow between populations increases as distance between populations decreases. -from Authors
Species' range expansions in response to climate change, and the invasion of exotic organisms, are two of the most pressing issues in ecology. Range expansions have already been documented in several taxa, including butterflies, grasshoppers and crickets, and birds, and as climate continues to change we can expect the ranges of many species to alter. Invasion of exotic organisms is of great interest currently because of the damage caused by many invasive species. Within a model, we find that during range expansion, selection generally favours individuals with a higher propensity for dispersal. This character change results in a more rapid spread than expected assuming evolutionary stasis. We show that Allee effects can slow invasion by reducing both selection for increased dispersal and chance of survival for propagules beyond the current range. Understanding how dispersal and other characters might evolve at expanding range margins is important not only for the prediction of range shifts in response to anthropogenic climate change, but also for understanding range shifting during previous natural climate change and for assessing the likely invasion dynamics of an introduced species.
We test the adaptive value of clutch size observed in a natural population of the chestnut weevil Curculio elephas. Clutch size is defined as the number of immatures per infested chestnut. In natural conditions, clutch size averages 1.7
eggs. By manipulating clutch size in the field, we demonstrate that deviations from the theoretical ”Lack clutch size”, estimated
as eight immatures, are mainly due to proximate and delayed effects of clutch size on offspring performance. We show the existence
of a trade-off between clutch size and larval weight. The latter, a key life-history trait, is highly correlated with fitness
because it is a strong determinant of larval survival and potential fecundity of offspring females. The fitness of different
potential oviposition strategies characterized by their clutch sizes, ranging from one to nine immatures, was calculated from
field- estimated parameters. Chestnut weevil females obtain an evolutionary advantage by laying their eggs singly, since,
for instance, fitness of single-egg clutches exceeds fitness of two-egg clutches and four-egg clutches by 8.0% and 15.1% respectively.
Conservation biology needs to be concerned not just with exogenous threats to populations, but also with the changing nature
of populations themselves. In a previous review paper, we highlighted evolution in contemporary time (years to decades) as
a largely overlooked aspect of population responses to environmental perturbations. We argued that these responses might affect
the fate of natural, managed and exotic populations. In the present review, we discuss issues that may limit the integration
of contemporary evolution into conservation biology—with the intent that recognition of these limitations may foster research,
discussion and resolution. In particular, we consider (1) alternative perceptions of “evolutionary” and “ecological” time,
(2) the role of contemporary evolution as an ecological process, (3) fitness as a bridge between evolution and conservation,
and (4) challenges faced by conservation strategies based on gene flow estimation or manipulation. We close by highlighting
some situations in which current conservation approaches and contemporary evolution may require reconciliation.
Dispersal is a key component of a species's ecology and will be under different selection pressures in different parts of the range. For example, a long-distance dispersal strategy suitable for continuous habitat at the range core might not be favoured at the margin, where the habitat is sparse. Using a spatially explicit, individual-based, evolutionary simulation model, the dispersal strategies of an organism that has only one dispersal event in its lifetime, such as a plant or sessile animal, are considered. Within the model, removing habitat, increasing habitat turnover, increasing the cost of dispersal, reducing habitat quality or altering vital rates imposes range limits. In most cases, there is a clear change in the dispersal strategies across the range, although increasing death rate towards the margin has little impact on evolved dispersal strategy across the range. Habitat turnover, reduced birth rate and reduced habitat quality all increase evolved dispersal distances at the margin, while increased cost of dispersal and reduced habitat density lead to lower evolved dispersal distances at the margins. As climate change shifts suitable habitat poleward, species ranges will also start to shift, and it will be the dispersal capabilities of marginal populations, rather than core populations, that will influence the rate of range shifting.
In classical evolutionary theory, traits evolve because they facilitate organismal survival and/or reproduction. We discuss a different type of evolutionary mechanism that relies upon differential dispersal. Traits that enhance rates of dispersal inevitably accumulate at expanding range edges, and assortative mating between fast-dispersing individuals at the invasion front results in an evolutionary increase in dispersal rates in successive generations. This cumulative process (which we dub "spatial sorting") generates novel phenotypes that are adept at rapid dispersal, irrespective of how the underlying genes affect an organism's survival or its reproductive success. Although the concept is not original with us, its revolutionary implications for evolutionary theory have been overlooked. A range of biological phenomena (e.g., acceleration of invasion fronts, insular flightlessness, preadaptation) may have evolved via spatial sorting as well as (or rather than) by natural selection, and this evolutionary mechanism warrants further study.
Many parasites affect the viability of their hosts, but detailed studies combining empirical data from both the field and the laboratory are limited. Consequently, the nature and magnitude of such effects are poorly known for many important host-parasite systems, including macroparasites of amphibians. We examined the effects of lungworm (Rhabdias pseudosphaerocephala) infections in cane toads (Bufo marinus) within their invasive Australian range. The host-specificity of this parasite suggests that it might serve as a biological control agent for toads in Australia, if infection proves to reduce toad viability. Mark-recapture studies in the field (near Darwin, Northern Territory) revealed lowered growth rates in infected adult toads when compared to uninfected toads, and a laboratory experiment confirmed causality: experimental infection with R. pseudosphaerocephala reduce toad growth rates. In combination with previous work on the current host-parasite system, it is now evident that nematode lungworms reduce the viability of both newly metamorphosed and adult cane toads, and do so in the field as well as in the laboratory. Rhabdias pseudosphaerocephala may be a valuable component of a biological control strategy for cane toads in Australia.
Host-parasite systems have often evolved over time, such that infection dynamics may become greatly modified from the time of initial contact of the host with the parasite. Biological invasions may be useful to clarify processes in the initial contact of hosts with parasites, and allow us to compare parasite uptake between the ancestral (coevolved) host and novel (noncoevolved) hosts. Cane toads (Bufo marinus) are spreading rapidly through tropical Australia, carrying with them a nematode lungworm (Rhabdias pseudosphaerocephala) congeneric with those found in Australian frogs. We investigated the dynamics of infections of the toad parasite by conducting histologic examinations of cane toads and three native Australian frogs (Litoria dahlii, Litoria nasuta, and Opisthodon ornatus) at 2, 6, and 10 days after experimental exposure to the toad lungworm. More worms were found in toads than in frogs, especially at longer periods postexposure. In toads, the infective larvae entered the skin and muscles within 2 days postexposure, passed into the coelom in 6 days, and reached the lungs at 10 days. In frogs, larvae were found in many organs rather than migrating to consistent target tissues; a few larvae reached the lungs of L. dahlii. Migratory larvae caused increasing inflammation (primarily granulomatous admixed with granulocytes then lymphocytes) through time, especially in frogs. Evolution has resulted in an enhanced ability of the lungworm to locate the target organ (the lungs) of the toad, and an increase in rates of parasite survival within this host.
The process of rapid range expansion (as seen in many invasive species, and in taxa responding to climate change) may substantially disrupt host-parasite dynamics. Parasites and pathogens can have strong regulatory effects on their host population and, in doing so, exert selection pressure on host life history. We construct a simple individual-based model of host-parasite dynamics during range expansion. This model shows that the parasites and pathogens of a range-expanding host are likely to be absent from the host's invasion front, because stochastic events (serial founder events) in low-density frontal populations result in local extinctions or transmission failure of the parasite/pathogen and, hence, a preponderance of uninfected hosts in the invasion vanguard. This pattern is true for both density-dependent and density-independent transmission rates, although it is exacerbated in the case of density-dependent transmission because, in this case, transmission rates also decline on the front. Data from field surveys on the prevalence of lungworms (Rhabdias pseudosphaerocephala) in invasive cane toads (Bufo marinus) support these predictions, in showing that toads in newly invaded areas of tropical Australia lack the parasite, which only arrives 1-3 years after the toads themselves. The resultant "honeymoon phase" immediately post-invasion, when individuals in the invasion-front population are virtually pathogen-free, may lead to altered host population dynamics on the invasion front, causing, for example, high densities in invasion-front populations, followed by a decline in numbers as parasites and pathogens arrive and begin to reduce host viability. The honeymoon phase may ultimately impact the evolution of life-history investment strategies in both host and parasite on the invasion vanguard, as hosts are released from immune challenges and parasites continuously expand into a favorable and unoccupied niche.
Individuals in the vanguard of a species invasion face altered selective conditions when compared with conspecifics behind the invasion front. Assortment by dispersal ability on the expanding front, for example, drives the evolution of increased dispersal, which, in turn, leads to accelerated rates of invasion. Here I propose an additional evolutionary mechanism to explain accelerating invasions: shifts in population growth rate (r). Because individuals in the vanguard face lower population density than those in established populations, they should (relative to individuals in established populations) experience greater r-selection. To test this possibility, I used the ongoing invasion of cane toads (Bufo marinus) across northern Australia. Life-history theory shows that the most efficient way to increase the rate of population growth is to reproduce earlier. Thus, I predict that toads on the invasion front will exhibit faster individual growth rates (and thus will reach breeding size earlier) than those from older populations. Using a common garden design, I show that this is indeed the case: both tadpoles and juvenile toads from frontal populations grow around 30 per cent faster than those from older, long established populations. These results support theoretical predictions that r increases during range advance and highlight the importance of understanding the evolution of life history during range advance.
Cane toads (Bufo marinus) were introduced to Australia in 1935 and have since spread widely over the continent, generating concern regarding ecological impacts on native predators. Most Australian cane toad populations are infected with lung nematodes Rhabdias pseudosphaerocephala, a parasite endemic to New World (native-range) cane toad populations; presumably introduced to Australia with its toad host. Considering the high intensities and prevalence reached by this parasite in Australian toad populations, and public ardour for developing a control plan for the invasive host species, the lack of experimental studies on this host-parasite system is surprising. To investigate the extent to which this lungworm influences cane toad viability, we experimentally infected metamorph toads (the smallest and presumably most vulnerable terrestrial phase of the anuran life cycle) with the helminth. Infected toads exhibited reduced survival and growth rates, impaired locomotor performance (both speed and endurance), and reduced prey intake. In summary, R. pseudosphaerocephala can substantially reduce the viability of metamorph cane toads.
Several epidemiological models predict a positive relationship between host population density and abundance of directly transmitted macroparasites. Here, we generalize these, and test the prediction by a comparative study. We used data on communities of gastrointestinal strongylid nematodes from 19 mammalian species, representing examination of 6670 individual hosts. We studied both the average abundance of all strongylid nematodes within a host species, and the two components of abundance, prevalence and intensity. The effects of host body weight, diet, fecundity and age at maturity and parasite body size were controlled for directly, and the phylogenetically independent contrast method was used to control for confounding factors more generally. Host population density and average parasite abundance were strongly positively correlated within mammalian taxa, and across all species when the effects of host body weight were controlled for. Controlling for other variables did not change this. Even when looking at single parasite species occurring in several host species, abundance was highest in the host species with the highest population density. Prevalence and intensity showed similar patterns. These patterns provide the first macroecological evidence consistent with the prediction that transmission rates depend on host population density in natural parasite communities.
Numerous studies of wild populations have shown that phenotypic traits can change adaptively on short timescales, but very few studies have considered coincident changes in major fitness components. We here examine adaptive changes in life-history traits and survival rates for wild guppies introduced into new environments. Female life-history traits in the derived (Damier River) populations diverged from the ancestral (Yarra River) population, as a result of adaptation to predation regime (high vs. low) and other aspects of the local river. Moreover, some components of the derived Damier populations, particularly juveniles, now show higher survival in the Damier than do contemporary representatives from the ancestral Yarra population. These results suggest that adaptive change can improve survival rates after fewer than 10 years (fewer than 30 guppy generations) in a new environment.
The present study used experimental infections to compare the life cycles and life histories of 6 Rhabdias spp. infecting snakes and anurans. Free-living development of anuran lungworms was primarily limited to heterogonic reproduction, and females utilized matricidal endotoky exclusively, whereas snake lungworms primarily reproduced homogonically and, when heterogonic reproduction occurred, females used a combination of releasing eggs and matricidal endotoky. Infective snake lungworms survived for longer periods in fresh water compared to anuran worms. Infective anuran lungworms penetrated into the skin of frogs and toads; few infections resulted from per os infections. In contrast, snake lungworms were unable to penetrate skin; instead, infective juveniles penetrated into snake esophageal tissue during per os infections. Despite separate points of entry, anuran and snake lungworms both migrated and developed in the fascia, eventually penetrating into the body cavity of the host. Worms molted to adulthood inside the body cavity and subsequently penetrated into the host's lungs, where they fed on blood while becoming gravid. Adult lungworm survival varied among lungworm species, but, in general, snake lungworms were longer lived than anuran worms. Anuran lungworms were poorly suited for transmission via transport hosts, whereas snake lungworms were consistently capable of establishing infections using transport hosts. Overall, these observations suggest that snake and anuran lungworms have discrepant life cycles and life history strategies.
Life history theory tries to explain how evolution designs organisms to achieve reproductive success. The design is a solution to an ecological problem posed by the environment and subject to constraints intrinsic to the organism. Work on life histories has expanded the role of phenotypes in evolutionary theory, extending the range of predictions from genetic patterns to whole-organism traits directly connected to fitness. Among the questions answered are the following: Why are organisms small or large? Why do they mature early or late? Why do they have few or many offspring? Why do they have a short or a long life? Why must they grow old and die? The classical approach to life histories was optimization; it has had some convincing empirical success. Recently non-equilibrium approaches involving frequency-dependence, density-dependence, evolutionary game theory, adaptive dynamics, and explicit population dynamics have supplanted optimization as the preferred approach. They have not yet had as much empirical success, but there are logical reasons to prefer them, and they may soon extend the impact of life history theory into population dynamics and interspecific interactions in coevolving communities.
Cane toads (Bufo marinus) are large anurans (weighing up to 2 kg) that were introduced to Australia 70 years ago to control insect pests in sugar-cane fields. But the result has been disastrous because the toads are toxic and highly invasive. Here we show that the annual rate of progress of the toad invasion front has increased about fivefold since the toads first arrived; we find that toads with longer legs can not only move faster and are the first to arrive in new areas, but also that those at the front have longer legs than toads in older (long-established) populations. The disaster looks set to turn into an ecological nightmare because of the negative effects invasive species can have on native ecosystems; over many generations, rates of invasion will be accelerated owing to rapid adaptive change in the invader, with continual 'spatial selection' at the expanding front favouring traits that increase the toads' dispersal.
Evolutionary ecology predicts that parasite life-history traits, including a parasite's survivorship and fecundity within a host, will evolve in response to selection and that their evolution will be constrained by trade-offs between traits. Here, we test these predictions using a nematode parasite of rats, Strongyloides ratti, as a model. We performed a selection experiment by passage of parasite progeny from either early in an infection ('fast' lines) or late in an infection ('slow' lines). We found that parasite fecundity responded to selection but that parasite survivorship did not. We found a trade-off mediated via conspecific density-dependent constraints; namely, that fast lines exhibit higher density-independent fecundity than slow lines, but fast lines suffered greater reduction in fecundity in the presence of density-dependent constraints than slow lines. We also found that slow lines both stimulate a higher level of IgG1, which is a marker for a Th2-type immune response, and show less of a reduction in fecundity in response to IgG1 levels than for fast lines. Our results confirm the general prediction that parasite life-history traits can evolve in response to selection and indicate that such evolutionary responses may have significant implications for the epidemiology of infectious disease.
Two new Rhabdias species are described from the lungs of the cane toad Bufo marinus (L.) from Costa Rica and Nicaragua. Rhabdias alabialis n. sp. differs from other known species of the genus by the remarkable morphology of its head end, i.e., the absence of lips or pseudolabia, the slitlike oral opening, and the triangular shape of the buccal capsule in apical view. Rhabdias pseudosphaerocephala n. sp. is identified as a form previously known in Central and South America as Rhabdias sphaerocephala Goodey, 1924, a species initially described from toads in Europe. The new species is differentiated from R. sphaerocephala based on head-end morphology and sequences of nuclear rDNA.
To predict the spread of invasive species, we need to understand the mechanisms that underlie their range expansion. Assuming random diffusion through homogeneous environments, invasions are expected to progress at a constant rate. However, environmental heterogeneity is expected to alter diffusion rates, especially by slowing invasions as populations encounter suboptimal environmental conditions. Here, we examine how environmental and landscape factors affect the local invasion speeds of cane toads (Chaunus [Bufo] marinus) in Australia. Using high-resolution cane toad data, we demonstrate heterogeneous regional invasion dynamics that include both decelerating and accelerating range expansions. Toad invasion speed increased in regions characterized by high temperatures, heterogeneous topography, low elevations, dense road networks, and high patch connectivity. Regional increases in the toad invasion rate might be caused by environmental conditions that facilitate toad reproduction and movement, by the evolution of long-distance dispersal ability, or by some combination of these factors. In any case, theoretical predictions that neglect environmental influences on dispersal at multiple spatial scales may prove to be inaccurate. Early predictions of cane toad range expansion rates that assumed constant diffusion across homogeneous landscapes already have been proved wrong. Future attempts to predict range dynamics for invasive species should consider heterogeneity in (1) the environmental factors that determine dispersal rates and (2) the mobility of invasive populations because dispersal-relevant traits can evolve in exotic habitats. As an invasive species spreads, it is likely to encounter conditions that influence dispersal rates via one or both of these mechanisms.
Using data on 66 species from 18 families and 6 orders, we examine patterns of interspecific covariation in female size, egg size, time from infection to production of infective stages (prepatency period), duration of reproduction (patency period), and fecundity in mammalian intestinal nematodes. Nematode species with shorter prepatency periods are smaller, have lower rates of somatic growth, lower fecundity and shorter reproductive periods; those with longer prepatency periods have the opposite suite of characters. These patterns are very different from that found in interspecific analyses of life history variation in other taxa. This may be a consequence of the energy-rich environment intestinal nematodes exploit, though comparable studies of free-living nematodes or other soft-bodies invertebrate phyla have not yet been done. The advantages of delaying reproduction, with the subsequent increase in fecundity and reproductive lifespan, depend on a number of factors, such as the relative importance of prepatency in the determination of parasite generation times, and adult mortality rates. Contrary to previous claims, nematode egg size is shown to be highly variable (as variable as female size), yet this variation is not associated with any other component of reproductive rate. This may be because of interspecific variation in egg shell thickness and complexity.
The population structure of the mycophagous beetle P. substriatus is characterized by many small local populations interconnected by migration over a small spatial scale (10×75 m2). Each local P. substriatus population has a relatively short expected persistence time, but persistence of the species occurs due to a balance between frequent local extinctions and recolonizations. This non-equilibrium population structure can have profound effects on how the genetic variation is structured between and within populations. Theoretical models have stated that the genetic differentiation among local populations will be enhanced relative to an island model at equilibrium if the number of colonizers is less than approximately twice the number of migrants among local populations. To study these effects, a set of 50 local P. substriatus populations were surveyed over a four year period to record any naturally occurring extinctions and recolonizations. The per population colonization and extinction rate were 0.237 and 0275, respectively. Mark-recapture techniques were used to estimate a number of demographic parameters: local population size (N=11.1), migration rate (=0.366), number of colonizers (k=4.0) and the probability of common origin of colonizers (φ=0.5). The theoretically predicted level of differentiation among local populations (measured as Wright’s FST) was 0.070. Genetic data obtained from an electrophoretic survey of 7 polymorphic loci gave an estimated degree of differentiation of 0.077. There was thus a good agreement between the empirical results and the theoretical predictions. Young populations (young=0.090) had significantly higher levels of differentiation than old, more established populations (old=0.059). The extinction-recolonization dynamics resulted in an overall increased in the genetic differentiation among local populations by c. 40%. The overall effective population size was also reduced by c. 35%. The results give clear evidence to how non-equilibrium processes shape the genetic structure of populations.
We develop an optimality model based on classical epidemiological models to investigate the optimal time to patency in parasitic nematodes in relation to host mortality and parasite mortality. We found that the optimal time to patency depends on both host longevity and prepatent mortality of nematodes. We tested our models using a comparative analysis of the relationships between nematode time to patency, nematode mortality and host mortality. Although we confirmed the importance of prepatent mortality, we also found a significant positive influence of host mortality. Host mortality rate affects parasite survivorship and life history strategies in the same way that habitat-specific mortality regimes drive the evolution of life histories in free-living organisms.
Free-living development of Rhabdias americanus and Rhabdias ranae was heterogonic and development of infective larvae was by matricidal endotoky. Both species were experimentally transmitted by skin penetration. Development of R. americanus in Bufo americanus and R. ranae in Rana sylvatica was similar. Growth of third- and fourth-stage larvae occurred in fascia and muscle tissue of the host during migration to the body cavity. Adult worms were recovered only from the body cavity and lungs; larvae were never observed in these locations. Worms probably entered the lungs by direct penetration. Gravid nematodes were observed only in the lungs. Both R. americanus and R. ranae were transmitted to toad and frog tadpoles, respectively, and worms developed to adulthood in tadpoles. Terrestrial snails (Oxyloma decampi Tryon and Discus cronkhitei Newcomb) were demonstrated as possible paratenic hosts for R. americanus. Rhabdias americanus, which does not occur in frogs, and R. ranae, which does not occur in toads in the wild at Guelph, were experimentally cross-transmitted to these amphibians and developed successfully to adults. Infective larvae of these species, however, did not as readily penetrate into the unusual host as the usual host. It is suggested that ecological barriers have prevented cross infections in the wild.
Despite the importance of reproduction in platyhelminth parasite biology, there is generally only sketchy information on key parameters; many studies lack documentation on variation and there is limited application of laboratory studies to natural events. This review focuses on case studies involving monogeneans (species of the genera Polystoma, Protopolystoma, Pseudodiplorchis, Discocotyle, and Gyrodactylus) where laboratory experimental data are linked with fieldwork to produce exact measurements of life-history traits. Data are characterized by wide variation and sensitivity to limiting factors. In contrasting patterns of reproductive biology, controls are imposed by the external environment and by density, but there is consistent evidence of powerful regulation by host factors; most reproductive parameters, including prepatent period, egg production rate, and life-span, are negatively affected. Alongside rate-limiting effects, host factors operating during prereproductive development inflict massive mortality; this strongly regulates the size of the adult parasite population contributing to future recruitment. High fecundity is traditionally viewed as compensating for losses that occur as a result of the hazards of transmission, but this review suggests that parasite reproductive adaptations have their most significant role in countering the additional losses that occur post invasion. Regulation of parasite reproductive potential by host immunity and the reproductive specializations that counter this constraint represent a distinguishing characteristic of parasitism.
1. Species would be expected to shift northwards in response to current climate warming, but many are failing to do so because of fragmentation of breeding habitats. Dispersal is important for colonisation and an individual‐based spatially explicit model was developed to investigate impacts of habitat availability on the evolution of dispersal in expanding populations. Model output was compared with field data from the speckled wood butterfly Pararge aegeria , which currently is expanding its range in Britain.
2. During range expansion, models simulated positive linear relationships between dispersal and distance from the seed location. This pattern was observed regardless of quantity (100% to 10% habitat availability) or distribution (random vs. gradient distribution) of habitat, although highe