Martin Reichard

Rapid growth, early maturation and short generation time in African annual fishes.

BackgroundExtreme environmental conditions can give rise to extreme adaptations. We document growth, sexual maturation and fecundity in two species of African annual fish inhabiting temporary savanna pools.ResultsNothobranchius kadleci started to reproduce at the age of 17 days and size of 31 mm and Nothobranchius furzeri at 18 days and 32 mm. All four study populations demonstrated rapid growth rates of up to 2.72 mm/day (23.4% of their total length). Both species may produce diapausing embryos or embryos that are able to hatch in as few as 15 days, resulting in a minimum generation time as short as only one month. Incubation on the surface of damp peat moss results in high embryo survival (73%) and a high proportion of rapidly developing embryos (58%) that skip diapauses and hatch in less than 30 days. We further demonstrated that rapid growth and maturation do not compromise subsequent fecundity.ConclusionsOur data suggest that both species have the most rapid sexual maturation and minimum generation time of any vertebrate species, and that rapid maturity does not involve paedogenesis.

Sexual selection for male dominance reduces opportunities for female mate choice in the European bitterling (Rhodeus sericeus)

Sexual selection involves two main mechanisms: intrasexual competition for mates and intersexual mate choice. We experimentally separated intrasexual (male–male interference competition) and intersexual (female choice) components of sexual selection in a freshwater fish, the European bitterling (Rhodeus sericeus). We compared the roles of multiple morphological and behavioural traits in male success in both components of sexual competition, and their relation to male reproductive success, measured as paternity of offspring. Body size was important for both female choice and male–male competition, though females also preferred males that courted more vigorously. However, dominant males often monopolized females regardless of female preference. Subordinate males were not excluded from reproduction and sired some offspring, possibly through sneaked ejaculations. Male dominance and a greater intensity of carotenoid‐based red colouration in their iris were the best predictors of male reproductive success. The extent of red iris colouration and parasite load did not have significant effects on female choice, male dominance or male reproductive success. No effect of parasite load on the expression of red eye colouration was detected, though this may have been due to low parasite prevalence in males overall. In conclusion, we showed that even though larger body size was favoured in both intersexual and intrasexual selection, male–male interference competition reduced opportunities for female choice. Females, despite being choosy, had limited control over the paternity of their offspring. Our study highlights the need for reliable measures of male reproductive success in studies of sexual selection.

Distribution, colour polymorphism and habitat use of the African killifish Nothobranchius furzeri, the vertebrate with the shortest life span

Intensive collection in southern Mozambique across and outside the potential range of Nothobranchius furzeri, the species with the shortest recorded life span among vertebrates used as a model in ageing research, revealed that, contrary to previous data, it is a widespread species. It occurs in small freshwater pools south of the Save River and north of the Incomati River, including basins of the Limpopo, Changane, Chefu, Mazimechopes and Vaneteze Rivers. During collection in February 2008 (the second part of the rainy season), populations were strongly female biased (mean, 28% of males across 19 populations), and there was a spatial pattern in female bias among metapopulations. Populations varied in the proportion of male colour morphs. Fourteen populations were composed exclusively of the red male phenotype, three populations of the yellow male phenotype and 12 populations were mixed. Overall, the red phenotype was more common, but there was strong geographical variation in morph proportion, with yellow males more abundant at the periphery and red male dominance in the centre of the range of N. furzeri in the Limpopo basin. Nothobranchius furzeri was sympatric with Nothobranchius orthonotus (35% of investigated pools) and Nothobranchius rachovii (27% of sites). Analysis of habitat use of N. furzeri is presented; N. furzeri was associated with pools containing a soft muddy substratum and turbid water.

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.

Parallel evolution of senescence in annual fishes in response to extrinsic mortality

BackgroundEarly evolutionary theories of aging predict that populations which experience low extrinsic mortality evolve a retarded onset of senescence. Experimental support for this theory in vertebrates is scarce, in part for the difficulty of quantifying extrinsic mortality and its condition- and density-dependent components that –when considered- can lead to predictions markedly different to those of the “classical” theories. Here, we study annual fish of the genus Nothobranchius whose maximum lifespan is dictated by the duration of the water bodies they inhabit. Different populations of annual fish do not experience different strengths of extrinsic mortality throughout their life span, but are subject to differential timing (and predictability) of a sudden habitat cessation. In this respect, our study allows testing how aging evolves in natural environments when populations vary in the prospect of survival, but condition-dependent survival has a limited effect. We use 10 Nothobranchius populations from seasonal pools that differ in their duration to test how this parameter affects longevity and aging in two independent clades of these annual fishes.ResultsWe found that replicated populations from a dry region showed markedly shorter captive lifespan than populations from a humid region. Shorter lifespan correlated with accelerated accumulation of lipofuscin (an established age marker) in both clades. Analysis of wild individuals confirmed that fish from drier habitats accumulate lipofuscin faster also under natural conditions. This indicates faster physiological deterioration in shorter-lived populations.ConclusionsOur data provide a strong quantitative example of how extrinsic mortality can shape evolution of senescence in a vertebrate clade. Nothobranchius is emerging as a genomic model species. The characterization of pairs of closely related species with different longevities should provide a powerful paradigm for the identification of genetic variations responsible for evolution of senescence in natural populations.

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.

Age structure of annual Nothobranchius fishes in Mozambique: is there a hatching synchrony?

The age structures of populations of African annual Nothobranchius spp. were examined for the first time. Daily increments in sagittal otoliths of Nothobranchius furzeri, Nothobranchius kadleci, Nothobranchius orthonotus and Nothobranchius rachovii from southern and central Mozambique were used for age determination. Four hypotheses were tested: (1) timing of hatching is consistent with the calendar onset of the rainy season, (2) hatching is synchronized within a population in a pool, (3) there is a difference in hatching date between geographical regions differing in mean total annual precipitation and (4) sympatric Nothobranchius spp. hatch at the same time. The results show that daily increment analysis represents an applicable method for age determination in Nothobranchius spp. Despite a significant positive relationship between age and size of fishes, a pronounced variation in fish size at an age precluded the use of fish size as a valid age marker. Timing of hatching was not consistent with the calendar onset of the rainy season. Interpopulation variability was observed in the degree of hatching date synchronization within a population. Hatching dates were relatively uniform in some populations, while there was considerable variability in others. Differences in timing of hatching date were found in only 1 of 2 years within the three regions investigated (Chefu, lower Limpopo and Sofala regions), each of which differed in mean total annual rainfall. The hatching dates of sympatric Nothobranchius spp. were marginally different, but further testing on a larger sample is needed for conclusive results.

Spatial distribution of drifting cyprinid fishes in a shallow lowland river

We investigated downstream drift of the early developmental stages of cyp- rinid fishes in a shallow lowland river to ascertain the spatial dynamics of this mode of transport. Drift density and mean body size were compared among four sampling sta- tions positioned at different distances from the riverbank through a series of diel sam- pling periods. Common bream ( Abramis brama ) was the dominant species (76%), fol- lowed by silver bream ( Abramis bjoerkna ) and roach (Rutilus rutilus ). Ninety-five per- cent of drifting fish were larvae. Most fish drifted 1 to 3m from the shore, at a max- imum density of 131 fish 100m -3 . Relatively few fish drifted in midchannel and most fish drifted at night. Body size of drifting fishes was positively correlated with distance from the bank. Consistent results were obtained from analysis of developmental sta- ges, with younger larvae drifting near to the bank and older larvae and early juveniles drifting in midchannel. We propose that the spatial distribution of drifting fish is linked to their swimming ability and fish larvae may enter the river current as a means of ac- tive transport.

Phylogeny, genetic variability and colour polymorphism of an emerging animal model: The short-lived annual Nothobranchius fishes from southern Mozambique

Nothobranchius are a group of small, extremely short-lived killifishes living in temporary savannah pools in Eastern Africa and that survive annual desiccation of their habitat as dormant eggs encased in dry mud. One mitochondrial (COI) and three nuclear (CX32.2, GHITM, PNP) loci were used to investigate the phylogenetic relationship of Nothobranchius species from southern and central Mozambique. This group shows marked variation in captive lifespan at both the inter- and intraspecific levels; lifespan varies from a few months to over a year. As their distribution encompasses a steep gradient between semi-arid and humid habitats, resulting in contrasting selection pressures on evolution of lifespan and associated life history traits, Mozambican Nothobranchius spp. have recently become a model group in studies of ageing, age-related disorders and life history evolution. Consequently, intraspecific genetic variation and male colour morph distribution was also examined in the recovered clades. Using Bayesian species tree reconstruction and single loci analyses, three large clades were apparent and their phylogenetic substructure was revealed at the inter- and intra-specific levels within those clades. The Nothobranchius furzeri and Nothobranchius orthonotus clades were strongly geographically structured. Further, it was demonstrated that male colour has no phylogenetic signal in N. furzeri, where colour morphs are sympatric, but is associated with two reciprocally monophyletic groups in Nothobranchius rachovii clade, where colour morphs are parapatric. Finally, our analysis showed that a polymorphism in the Melanocortin1 receptor gene (which controls pigmentation in many vertebrates and was a candidate gene of male colouration in N. furzeri) is unrelated to colour phenotypes of the study species. Our results raise significant implications for future comparative studies of the species and populations analysed in the present work.

Seasonal change in the opportunity for sexual selection

Environmental and population parameters that influence the strength of sexual selection may vary considerably over the course of the reproductive season. However, the potential for sexual selection frequently fails to translate into variation in reproductive success among individuals. We investigated seasonal changes in variation in reproductive success, measured as the opportunity for sexual selection, using parentage analysis in 20 experimental populations of the European bitterling (Rhodeus amarus, Cyprinidae), a small freshwater fish with a promiscuous, resource‐based mating system. We showed that although the largest males sired most offspring over the entire reproductive season, variation in reproductive success and hence the opportunity for sexual selection was low at the start of the season but increased significantly at its end. This seasonal difference probably arose from the superior competitive endurance of large males and from a higher temporal clustering of reproductively active females at the start of the breeding season than later in the season. The spatial distribution of oviposition sites had a negligible effect on the variation in reproductive success. We discuss the potential implications of our results for the importance and strength of sexual selection in natural populations.