Milan Vrtílek

The role of host specificity in explaining the invasion success of the freshwater mussel Anodonta woodiana in Europe

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 that host availability does not constitute a major limit for A. woodiana to colonise most aquatic habitats in Central Europe. In addition, we investigated seasonal dynamics of A. woodiana reproduction and did not detect any limitations of its reproduction by ambient water temperatures typical of a Central European lowland river. Consequently, we predict that A. woodiana may further increase the speed and range of its invasion and we discuss possible consequences to native habitats and communities, especially to the endangered species of unionid mussels.

Alternative intrapopulation life-history strategies and their trade-offs in an African annual fish

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.

Female bias in the adult sex ratio of African annual fishes: interspecific differences, seasonal trends and environmental predictors

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.

An invasive species reverses the roles in a host-parasite relationship between bitterling fish and unionid mussels

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.

Repeated intraspecific divergence in life span and aging of African annual fishes along an aridity gradient.

Life span and aging 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 aging. However, among populations within species, high extrinsic mortality can lead to extended life span and slower aging 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 life spans 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 intraspecific divergence in life span and aging 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 aging and life‐history traits conformed with or contradicted the predictions for each species. These findings demonstrate that variation in life span and functional decline among natural populations are linked, genetically underpinned, and can evolve relatively rapidly.

Seasonal dynamics in community structure, abundance, body size and sex ratio in two species of Neotropical annual fishes

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.

Community assembly in Nothobranchius annual fishes: Nested patterns, environmental niche and biogeographic history

Abstract 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.

Female fecundity traits in wild populations of African annual fish: the role of the aridity gradient.

Abstract 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.

Hatching Date Variability In Wild Populations of Four Coexisting Species Of African Annual Fishes

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 1 year, but less synchrony in the other 2 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. Developmental Dynamics 246:827–837, 2017.

The role of energetic reserves during embryonic development of an annual killifish

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. Developmental Dynamics 246:838–847, 2017.