- Martin Reichard
Test the roles of (1) population-specific traits, (2) geographic variability, (3) complex interspecific interactions, and (4) microevolutionary processes in species interactions on invasion success; to predict success of individual populations to establishing in non-native areas
Research Item (21)
Background: Females can significantly improve their fitness by utilizing a range of maternal effects. Embryos of annual killifish survive the dry season in ephemeral pools encased in dry substrate for several months. Here, we experimentally test the association between energetic provisioning and maternally controlled duration of embryonic development in the African annual killifish Nothobranchius furzeri (Cyprinodontiformes). Results: We found that embryonic energetic reserves do not limit duration of development. However, differences in energetic reserves affect the size at which embryos hatched, with larger yolk size resulting in larger hatchling size. Conclusions: These findings suggest uncoupling of the two traits examined, i.e. embryonic energetic reserves and development duration, and emphasize the strong buffering role of diapause in the energetic balance of embryonic development in the annual killifish. This article is protected by copyright. All rights reserved.
The evolution of life history is shaped by life expectancy. Life-history traits coevolve, and optimal states for particular traits are constrained by trade-offs with other life-history traits. Life histories contrast among species, but may also diverge intraspecifically, at the level of populations. We studied the evolution of female reproductive allocation strategy, using natural populations of two sympatric species of African annual fishes, Nothobranchius furzeri and Nothobranchius orthonotus. These species inhabit pools in the Mozambican savanna that are formed in the rainy season and persist for only 2–10 months. Using 207 female N. furzeri from 11 populations and 243 female N. orthonotus from 14 populations, we tested the effects of genetic background (intraspecific lineage) and life expectancy (position on the aridity gradient determining maximum duration of their temporary habitat) on female fecundity traits. First, we found that variation in female body mass was small within populations, but varied considerably among populations. Second, we found that fecundity was largely defined by female body mass and that females spawned most of their eggs in the morning. Third, we found that the trade-off between egg size and egg number varied among lineages of N. furzeri and this outcome has been confirmed by data from two separate years. Overall, we demonstrate that local conditions were important determinants for Nothobranchius growth and fecundity and that eggs size in arid region was less limited by female fecundity than in humid region.
Phenotypic plasticity is an important mechanism to maximise fitness in unpredictable environments by fine-tuning phenotypes to a specific environmental setting. We used Nothobranchius furzeri, an African annual fish from temporary pools with erratic changes in habitat condition, to study changes in the allocation to growth and reproduction and to test the key trade-off between egg size and number. In an experimental setting, we quantitatively varied ration at two levels and over two time periods, including temporal switches in ration level. As predicted, female N. furzeri possessed the capacity for compensatory growth, which surprisingly came with no longer-term cost to fecundity. Females responded strongly to ration manipulation, with a pronounced decrease in fecundity associated with a low ration, even after accounting for body mass. Due to the unpredictability of offspring environment, we expected no adaptive change in oocyte size. However, females responded to the quality of their environment in accordance with an adaptive maternal effect, with females receiving a low ration producing larger eggs. Further, a switch in ration size in either direction was associated with a decrease in egg size. There was a trade-off between egg size and number in half of the treatments, but high variability in egg size among females made the relationship complex. Overall, N. furzeri females demonstrated high plasticity in both growth rate and fecundity parameters. Females appear able to track and respond adaptively to unpredictable changes in food availability in their environment.
Populations of annual killifish of the genus Nothobranchius occur in patchily distributed temporary pools in the East African savannah. Their fragmented distribution and low dispersal ability result in highly structured genetic clustering of their populations. In this study, we examined body shape variation in a widely distributed species, Nothobranchius orthonotus with known phylogeographic structure. We tested whether genetic divergence of major mitochondrial lineages forming two candidate species is congruent with phenotypic diversification, using linear and geometric morphometry analyses of body shape in 23 wild populations. We also conducted a common-garden experiment with two wild-derived populations to control for the effect of local environmental conditions on body shape. We identified different allometric trajectories for different mitochondrial lineages and candidate species in both sexes. However, in a principal components analysis of population-level body shape, the separation among mitochondrial lineages was incomplete. Higher similarity of mitochondrial lineages belonging to different candidate species than that of same candidate species prevented distinction of the two candidate species on the basis of body shape. Analysis at the individual level demonstrated that N. orthonotus express high intrapopulation variability, with major overlap among individuals from all populations. In conclusion, we suggest that N. orthonotus be considered as a single species with an extensive geographic range, strong population genetic structure and high morphological variability.
The impact of multiple invading species can be magnified owing to mutual facilitation--termed 'invasional meltdown'--but invasive species can also be adversely affected by their interactions with other invaders. Using a unique reciprocal host-parasite relationship between a bitterling fish (Rhodeus amarus) and unionid mussels, we show that an invasive mussel reverses the roles in the relationship. Bitterling lay their eggs into mussel gills, and mussel larvae parasitize fish. Bitterling recently colonized Europe and parasitize all sympatric European mussels, but are unable to use a recently invasive mussel, Anodonta woodiana. The parasitic larvae of A. woodiana successfully develop on R. amarus, whereas larvae of European mussels are rejected by bitterling. This demonstrates that invading species may temporarily benefit from a coevolutionary lag by exploiting evolutionarily naive hosts, but the resulting relaxed selection may facilitate its exploitation by subsequent invading species, leading to unexpected consequences for established interspecific relationships.
The natural history of model organisms is often overlooked despite its importance to correctly interpret the outcome of laboratory studies. Ageing is particularly understudied in natural populations. To address this gap, we present lifetime demographic data from wild populations of an annual species, the turquoise killifish, Nothobranchius furzeri, a model species in ageing research, and two other species of coexisting annual killifishes. Annual killifish hatch synchronously, have non-overlapping generations, and reproduce daily after reaching sexual maturity. Data from 13 isolated savanna pools in southern Mozambique demonstrate that the pools supporting killifish populations desiccated 1-4 months after their filling, though some pools persisted longer. Declines in population size over the season were stronger than predicted, because they exceeded the effect of steady habitat shrinking on population density that, contrary to the prediction, decreased. Populations of N. furzeri also became more female-biased with progressing season suggesting that males had lower survival. Nothobranchius community composition did not significantly vary across the season. Our data clearly demonstrate that natural populations of N. furzeri and its congeners suffer strong mortality throughout their lives, with apparent selective disappearance (condition-dependent mortality) at the individual level. This represents selective force that can shape the evolution of lifespan, and its variation across populations, beyond the effects of the gradient in habitat persistence.
- Aug 2018
Ephemeral habitats can impose challenging conditions for population persistence. Survival strategies in these environments can range from high dispersal capacity to the evolution of dormant stages able to tolerate a harsh environment outside the temporal window of favourable conditions . Annual killifish have evolved to live in seasonal pools on the African savannah and display a range of adaptations to cope with an unpredictable environment [2,3]. For most of the year, killifish populations survive as diapausing embryos buried in dry sediment. When savannah depressions fill with rainwater, the fish hatch, grow rapidly and, after attaining sexual maturity, reproduce daily [2,4]. Nothobranchius furzeri, a model species in ageing research [2,3], is distributed in a region where the climate is particularly dry and rains are unpredictable . Here, we demonstrate that the fast juvenile growth and rapid sexual maturation shown by N. furzeri in captivity is actually an underestimate of their natural developmental rate. We estimated the age of N. furzeri in natural populations by counting daily-deposited increments in the otoliths and performing histological analysis of gonads. We found that N. furzeri are capable of reaching sexual maturity within 14 days after hatching, which to our knowledge is the fastest rate of sexual maturation recorded for a vertebrate. We also demonstrate that N. furzeri can grow from an initial length of 5 mm up to 54 mm over the course of a two-week period. Such rapid juvenile development is likely to be adaptive since some pools were entirely desiccated 3-5 weeks after filling, but retained a viable killifish population that reproduced before the adults succumbed to the disappearance of their pool.
Predation and population density have fundamental size- and sex-specific effects on individual survival and demographic parameters. Given the overlap and interactions between different age cohorts in natural populations, separating the factors related to differential survival and growth based on longitudinal field-collected data is problematic. Using a Neotropical annual fish (Austrolebias minuano) with a single age cohort per generation, we used replicated field enclosures to experimentally test the roles of avian predation and fish population density on survival and growth over adult lifespan. We found that mortality risk was higher in larger males and smaller females when predation was experimentally excluded. Exposure to avian predation eliminated this sex-specific effect of body size on survival. No overall sex difference in survival was found in the experiment, despite a female-biased sex ratio in natural populations. Individually based growth rates were highest in enclosures at low population density with no predation risk. Overall, we demonstrate that annual fish suffer high sex-dependent size-specific mortality that is more strongly related to predation than to density-dependent processes. This has important implications for our understanding of the evolution of senescence and other life history traits in annual fishes.
Extreme asynchrony in embryo development, a typical feature of annual killifish living in temporary pools, represents a bet-hedging strategy to cope with unpredictable rainfall. African annual killifish are distributed across a large precipitation gradient, raising the potential for local adaptation in the degree of developmental asynchrony (e.g. higher in arid areas, lower in humid areas). Eight populations of two sister species, Nothobranchius furzeri and Nothobranchius kadleci, from sites along the rainfall gradient were tested and compared for asynchrony and duration of embryo development. Degree of asynchrony and mean duration of embryo development did not differ across the examined range. Despite generally high developmental variability, fish from more arid regions (where rain is more erratic) produced a significantly higher proportion of short-developing embryos. Comparable developmental asynchrony, regardless of precipitation level, suggests that all populations tested need to cope with some level of rainfall stochasticity. By producing more short-developing embryos, however, fish in more arid areas with relatively more erratic rains are better adapted to very short pool durations and are more likely to produce multiple offspring generations within a single rainy season.
Females can significantly improve their fitness by utilizing a range of maternal effects. Annual killifish are adapted to ephemeral pools, where only their embryos survive over several months long dry season encased in the desiccated substrate. The survival of prolonged embryonic development with limited resources available (yolk) is enabled by a series of developmental diapauses, when energetic metabolism is severely restricted. We experimentally tested the association between energetic provisioning and maternally controlled duration of embryonic development in the African annual killifish Nothobranchius furzeri (Cyprinodontiformes). We found that embryonic energetic reserves did not limit duration of the embryo development. However, the amount of initial energetic reserves affected the size at which embryos hatched, with larger yolk size resulting in larger hatchling size. These findings suggest uncoupling of the two traits examined, i.e. embryonic energetic reserves and development duration, and emphasize the strong buffering role of the diapause in the energetic balance of embryonic development of the annual killifish.
The assembly of local communities from regional species pools is shaped by historical aspects of distribution, environmental conditions, and biotic interactions. We studied local community assembly patterns in African annual killifishes of the genus Nothobranchius (Cyprinodontiformes), investigating data from 168 communities across the entire range of regionally co-existing species. Nothobranchius are small fishes associated with annually desiccating pools. We detected a nested pattern of local communities in one region (Southern Mozambique, with Nothobranchius furzeri as the core and dominant species), but no nestedness was found in the second region (Central Mozambique, with Nothobranchius orthonotus being the dominant species). A checkerboard pattern of local Nothobranchius community assembly was demonstrated in both regions. Multivariate environmental niche modeling revealed moderate differences in environmental niche occupancy between three monophyletic clades that largely co-occurred geographically and greater differences between strictly allopatric species within the clades. Most variation among species was observed along an altitudinal gradient; N. furzeri and Nothobranchius kadleci were absent from coastal plains, Nothobranchius pienaari, Nothobranchius rachovii, and Nothobranchius krysanovi were associated with lower altitude and N. orthonotus was intermediate and geographically most widespread species. We discuss implications for ecological and evolutionary research in this taxon.
Background: Hatching is modulated by a combination of intrinsic and extrinsic factors. Annual killifish are adapted to complete their entire life cycle in annually desiccating habitats. Spending most of their life in the embryonic stage, they have evolved adaptations to survive desiccated conditions and match their hatching with the unpredictable onset of the aquatic phase of the pool. We examined spatial and temporal synchrony of hatching in natural populations of four species of African annual killifish (genus Nothobranchius). We compared differences and variability in hatching dates among years, regions, pools and species and matched them with data on inundations of individual pools. Results: Inundations typically coincided with peak rainfall in early January. We found considerable spatial and temporal synchrony in one year, but less synchrony in the other two years. Hatching generally occurred 0-20 days after inundation; fish at most sites hatched synchronously (<1 week) but some sites showed protracted hatching or two age cohorts. One species tended to hatch earlier than the other three. Conclusions: We suggest that hatching of annual killifish in the wild is a result of the interplay between environmental conditions and individual predisposition to respond to threshold environmental cues, ensuring effective bet-hedging against unpredictable inundation. This article is protected by copyright. All rights reserved.
Lifespan and ageing are substantially modified by natural selection. Across species, higher extrinsic (environmentally-related) mortality (and hence shorter life expectancy) selects for the evolution of more rapid ageing. However, among populations within species, high extrinsic mortality can lead to extended lifespan and slower ageing as a consequence of condition-dependent survival. Using within-species contrasts of eight natural populations of Nothobranchius fishes in common garden experiments, we demonstrate that populations originating from dry regions (with short life expectancy) had shorter intrinsic lifespans and a greater increase in mortality with age, more pronounced cellular and physiological deterioration (oxidative damage, tumor load), and a faster decline in fertility than populations from wetter regions. This parallel intra-specific divergence in lifespan and ageing was not associated with divergence in early life history (rapid growth, maturation) or pace-of-life syndrome (high metabolic rates, active behavior). Variability across four study species suggests that a combination of different ageing and life history traits conformed with or contradicted the predictions for each species. These findings demonstrate that variation in lifespan and functional decline among natural populations are linked, genetically underpinned, and can evolve relatively rapidly. This article is protected by copyright. All rights reserved.
- Sep 2016
Seven ephemeral pools on the coastal plain of southern Brazil were found to be inhabited by three annual and 22 non-annual fish species. Two common annual species (Austrolebias minuano and Cynopoecilus fulgens) exhibited clear seasonal dynamics, with the appearance of young fishes in the austral autumn (May to June) and a decline in abundance over the seasonal cycle. The third annual species, Austrolebias wolterstorffii, was rare. No seasonal dynamics were observed in non-annual fishes. The relative abundance of non-annual fishes compared with annual fishes increased over the seasonal cycle, but they coexisted widely. The size structure of annual fishes suggested the presence of a single age cohort in most pools though a second age cohort was registered in one pool in August, coinciding with a large flooding. Strong sexual dimorphism in body size was found in C. fulgens throughout the seasonal cycle, while no sexual dimorphism in body size was found in A. minuano. Female-biased sex ratios were recorded in both common annual fish species in the last three sampling dates (in spring), but not during the first two sampling dates (in winter). The natural lifespan of annual fishes was <8 months. Annual fishes disappeared before habitat desiccation in half of the pools, while non-annual fishes were still present.
Figure S1. Logistic regression of Nothobranchius pool desiccation and position of the pool on the aridity gradient expressed by aridity index. Figure S2. Effect of sampling time on female spawning status. Table S1. Population characteristics including summary of female life‐history traits (mean ± SD) for the two studied Nothobranchius species. Table S2. Model‐averaged coefficient estimates for predictors of ovary mass. Table S3. Coefficient estimates for predictors of egg size.
Many populations have consistently biased adult sex ratios with important demographic and evolutionary consequences. However, geographical variation, the mechanisms, temporal dynamics and predictors of biased sex ratios are notoriously difficult to explain. We studied 334 wild populations of four species of African annual fish (Nothobranchius furzeri, N. kadleci, N. orthonotus, N. rachovii) across their ranges to compare their adult sex ratio, its seasonal dynamics, interpopulation variation and environmental predictors. Nothobranchius populations comprise a single age cohort and inhabit discrete isolated pools, with wide-ranging environmental conditions (habitat size, water turbidity, structural complexity, predators), making them ideal to study adult sex ratio variation. In captivity adult sex ratios were equal. In natural populations, adult sex ratios were biased 1:2 toward females in three study species while N. kadleci had sex ratios at unity. There was a decline in the proportion of males with age in one species, but not in the other species, implying most severe male mortality early after maturation, declining later perhaps with a decrease in male abundance. In general, the populations at vegetated sites had relatively more males than populations at sites with turbid water and little vegetation. Selective avian predation on brightly coloured male fish likely contributed to female dominance and vegetation cover may have protected males from birds. In addition, an aquatic predator, a large belastomid hemipteran, decreased the proportion of males in populations, possibly due to greater male activity rather than conspicuous colouration. Alternative explanations for a sex ratio bias, stemming from male-male contests for matings, are discussed. We conclude that the effect of environmental conditions on adult sex ratio varies dramatically even in closely related and ecologically similar sympatric species. Therefore, difficulties in explaining the ecological predictors of sex ratio biases are likely due to high stochasticity rather than limited sample size.
In ephemeral habitats, the same genotypes cope with unpredictable environmental conditions, favouring the evolution of developmental plasticity and alternative life-history strategies (ALHS). We tested the existence of intrapopulation ALHS in an annual killifish, Nothobranchius furzeri, inhabiting temporary pools. The pools are either primary (persisting throughout the whole rainy season) or secondary (refilled after desiccation of the initial pool), representing alternative niches. The unpredictable conditions led to the evolution of reproductive bet-hedging with asynchronous embryonic development. We used a common garden experiment to test whether the duration of embryonic period is associated with post-embryonic life-history traits. Fish with rapid embryonic development (secondary pool strategy, high risk of desiccation) produced phenotypes with more rapid life-history traits than fish with slow embryonic development (primary pool strategy). The fast fish were smaller at hatching but had larger yolk sac reserves. Their post-hatching growth was more rapid, and they matured earlier. Further, fast fish grew to a smaller body size and died earlier than slow fish. No differences in fecundity, propensity to mate or physiological ageing were found, demonstrating a combination of plastic responses and constraints. Such developmentally related within-population plasticity in life history is exceptional among vertebrates.
Invasive species represent a major threat with both direct and indirect effects on natural ecosystems, including effects on established and coevolved relationships. In a series of experiments, we examined how the interaction between two native species, a unionid mussel (Unio pictorum) and the European bitterling (Rhodeus amarus), a fish that parasitises unionids, was affected by the non-native zebra mussel (Dreissena polymorpha). The zebra mussel fouls hard substrates, including shells of living unionids, and its presence is often associated with a decrease in population density of native unionid mussels. Bitterling lay their eggs into live unionids and the embryos develop inside their gills. Using a range of zebra mussel densities, we demonstrated that zebra mussel fouling had a negative effect on the number of bitterling eggs inside the mussel host, with abundances of 5–10 zebra mussels (shell size 15–25 mm) per unionid critical for bitterling ability to utilise the host. In a further experiment, we found that bitterling did not discriminate between unfouled unionids and those fouled with five zebra mussels. Most ovipositions into fouled hosts, however, were unsuccessful as eggs failed to reach the unionid gills. We discuss implications of such unsuccessful ovipositions for bitterling recruitment and population dynamics.
Several freshwater mussel species represent some of the most problematic invasive species and have considerably altered ecosystems worldwide. Their invasion potential has been partially attributed to their free-living larvae, which have a high dispersal capability. We investigated the invasion potential of Anodonta (Sinanodonta) woodiana, a species of East Asian unionid mussel established worldwide despite having an obligatory parasitic stage (glochidium), which must encyst on host fish. The invasion success of A. woodiana has been attributed to the success of worldwide introductions of its sympatric fish hosts. We experimentally found, however, that A. woodiana is a broad host generalist, which can complete its development on all eight fish species tested, both coinvasive and native. Subsequently, we used a data on the occurrence and relative abundance of potential hosts in river habitats in the Czech Republic to project scenarios of the effect of host availability on A. woodiana invasion. We found th
Níže uvedené nálezy byly učiněny v průběhu terénního cvičení Ústavu botaniky a zoologie PřF MU Brno ve dnech 11.–16. září 2010. Navštívené lokality jsou řazeny chronologicky, tak jak byly prozkoumány. K jednotlivým lokalitám je uveden výčet nalezených druhů rostlin a živočichů, rozdělený do vyšších taxonomických jednotek. Faunisticky, floristicky či ochranářsky zajímavější nálezy jsou zvýrazněny tučným písmem a stručně komentovány. Také je uveden stupeň jejich ohrožení podle aktuálních červených seznamů (Holub & Procházka 2000, Farkač et al. 2005). Pokud není uvedeno jinak, byly fotky pořízeny účastníky terénní exkurze.