Reduced reproductive success of hatchery coho salmon in the wild: insights into most likely mechanisms

Supplementation of wild salmonids with captive-bred fish is a common practice for both commercial and conservation purposes. However, evidence for lower fitness of captive-reared fish relative to wild fish has accumulated in recent years, diminishing the apparent effectiveness of supplementation as a management tool. To date, the mechanism(s) responsible for these fitness declines remain unknown. In this study, we showed with molecular parentage analysis that hatchery coho salmon (Oncorhynchus kisutch) had lower reproductive success than wild fish once they reproduced in the wild. This effect was more pronounced in males than in same-aged females. Hatchery spawned fish that were released as unfed fry (age 0), as well as hatchery fish raised for one year in the hatchery (released as smolts, age 1), both experienced lower lifetime reproductive success (RS) than wild fish. However, the subset of hatchery males that returned as 2-year olds (jacks) did not exhibit the same fitness decrease as males that returned as 3-year olds. Thus, we report three lines of evidence pointing to the absence of sexual selection in the hatchery as a contributing mechanism for fitness declines of hatchery fish in the wild: (i) hatchery fish released as unfed fry that survived to adulthood still had low RS relative to wild fish, (ii) age-3 male hatchery fish consistently showed a lower relative RS than female hatchery fish (suggesting a role for sexual selection), and (iii) age-2 jacks, which use a sneaker mating strategy, did not show the same declines as 3-year olds, which compete differently for females (again, implicating sexual selection).     

Carry-over effect of captive breeding reduces reproductive fitness of wild-born descendants in the wild

Supplementation of wild populations with captive-bred organisms is a common practice for conservation of threatened wild populations. Yet it is largely unknown whether such programmes actually help population size recovery. While a negative genetic effect of captive breeding that decreases fitness of captive-bred organisms has been detected, there is no direct evidence for a carry-over effect of captive breeding in their wild-born descendants, which would drag down the fitness of the wild population in subsequent generations. In this study, we use genetic parentage assignments to reconstruct a pedigree and estimate reproductive fitness of the wild-born descendants of captive-bred parents in a supplemented population of steelhead trout (Oncorhynchus mykiss). The estimated fitness varied among years, but overall relative reproductive fitness was only 37 per cent in wild-born fish from two captive-bred parents and 87 per cent in those from one captive-bred and one wild parent (relative to those from two wild parents). Our results suggest a significant carry-over effect of captive breeding, which has negative influence on the size of the wild population in the generation after supplementation. In this population, the population fitness could have been 8 per cent higher if there was no carry-over effect during the study period.     

Pronounced reproductive skew in a natural population of green swordtails, Xiphophorus helleri

For many species in nature, a sire's progeny may be distributed among a few or many dams. This poses logistical challenges--typically much greater across males than across females--for assessing means and variances in mating success (number of mates) and reproductive success (number of progeny). Here we overcome these difficulties by exhaustively analyzing a population of green swordtail fish (Xiphophorus helleri) for genetic paternity (and maternity) using a suite of highly polymorphic microsatellite loci. Genetic analyses of 1476 progeny from 69 pregnant females and 158 candidate sires revealed pronounced skews in male reproductive success both within and among broods. These skews were statistically significant, greater than in females, and correlated in males but not in females with mating success. We also compare the standardized variances in swordtail reproductive success to the few such available estimates for other taxa, notably several mammal species with varied mating systems and degrees of sexual dimorphism. The comparison showed that the opportunity for selection on male X. helleri is among the highest yet reported in fishes, and it is intermediate compared to estimates available for mammals. This study is one of a few exhaustive genetic assessments of joint-sex parentage in a natural fish population, and results are relevant to the operation of sexual selection in this sexually dimorphic, high-fecundity species.     

The frequency and fitness consequences of communal breeding in a natural population of burying beetles: a test of reproductive skew

Abstract.  1. Reproductive cooperation occurs in diverse taxa and a defining characteristic of these social systems is how reproduction is shared. Both male and female burying beetles ( Nicrophorus spp.) facultatively form associations to bury a carcass and rear a single brood, making burying beetles a model system for testing skew theory.
2. In this study, 50% of 40–45 g carcasses and 75% of 55–60 g ones were buried by more than one male and/or female Nicrophorus tomentosus .
3. Females were significantly more likely to cooperate on 55–60 g carcasses than on 40–45 g ones.
4. Analysis of parentage of 13 broods using microsatellite loci as genetic markers showed that maternity analysis of only 2% of the young excluded all females captured leaving the brood chamber after burial. Males previously mated with resident females or displaced by resident males fathered 7% of the young.
5. The male and female remaining the longest were usually the parents of the most offspring, and reproductively dominant individuals also tended to be the largest.
6. Although all but two or three individuals that helped to bury the carcass produced some offspring, reproduction was often not shared equitably. Reproduction of females was significantly skewed on six of nine 40–45 g carcasses but shared fairly equitably on all three 55–60 g ones. Reproduction was skewed among males on 7 of 10 broods.
7. Both males and females relinquished a greater proportion of the brood as the days of assistance from all consexuals increased.     

Alternative male life-history tactics as potential vehicles for speeding introgression of farm salmon traits into wild populations

Releases of cultured organisms, such as farm Atlantic salmon (Salmo salar L.), threaten native biodiversity and the integrity of natural communities. Salmon escaping from sea farms, however, have relatively poor reproductive success, suggesting that the rate of spread of domesticated traits may be reduced. We now compare the relative reproductive success of males that mature precociously in freshwater (parr) and find that those of farm origin have higher breeding and fertilization success than wild and hybrid individuals. Specifically, hybrid parr had 57% and wild parr 25% the success of farm parr. Early maturing males could thus be important vehicles promoting introgression of domesticated and/or non‐native traits into wild populations and ultimately have long‐term impact on the genetic integrity of native populations.     

Impact of precocious male parr on the effective size of a wild population of Atlantic salmon

1. There is growing evidence that sexually mature but morphologically juvenile males of Atlantic salmon (precocious or mature male parr) actively participate in reproduction and, therefore, in the genetic composition of the populations of this species. The impact of mature male parr on the effective population size (N_e) of such populations has been previously studied under experimental settings, but no studies have been performed directly on natural populations. 2. Continuous monitoring and sampling of all sea returns is possible in the Lérez River (northwest of Spain). From demographic data on variances of reproductive success and genetic data from six microsatellite marker loci we carried out parentage assignment and assessed the impact of male parr on demographic and genetic estimates of N_e in two consecutive years. 3. Our results reveal that: (i) approximately 60% of the total sire paternity is attributable to mature parr; (ii) mature parr decrease the variance of reproductive success of males by a threefold factor and increase the effective population size of males by a 10‐fold factor; (iii) however, they do not substantially affect the variance of reproductive success and the effective size of females; (iv) mature parr increase two‐to threefold the overall effective size of the population but the ratio N_e/N, where N is the population size including or not mature parr in each case, is not affected.     

Microsatellite determination of male reproductive success in a natural population of the territorial ornate dragon lizard, Ctenophorus ornatus

It is now evident that the genetic mating system can be very different to the observed mating system. However, it is less well known what makes particular individuals more (or less) successful than expected from the observed system. In this study the observed territorial structure of a field population of the agamid lizard, Ctenophorus ornatus, was compared with the mating system as evidenced by microsatellite parentage assignment. This study also investigated whether any male traits predicted reproductive success. Sixty-five per cent of clutches were sired at least partially by a male other than the main territory-holding male and 35% of clutches were sired by a male with no overlap of the female's territory. Multiple paternity was moderately frequent at 25% of clutches. Male chest patch size predicted territory size and the number of females in the territory, but did not predict reproductive success. Instead, male head depth and body size were independently related to the number of offspring sired. As male head depth also predicted the number of females in a territory, these males are likely to be gaining increased reproductive success as a consequence of the higher number of females in their territories. Larger body size males, however, did not have a greater number of females in their territory and instead had more extra-territorial copulations. Whether these extra-territorial copulations are due to female choice or success in male competition is unknown.     

Time spent in distinct life history stages has sex‐specific effects on reproductive fitness in wild Atlantic salmon

In species with complex life cycles, life history theory predicts that fitness is affected by conditions encountered in previous life history stages. Here, we use a 4‐year pedigree to investigate if time spent in two distinct life history stages has sex‐specific reproductive fitness consequences in anadromous Atlantic salmon (Salmo salar). We determined the amount of years spent in fresh water as juveniles (freshwater age, FW, measured in years), and years spent in the marine environment as adults (sea age, SW, measured in sea winters) on 264 sexually mature adults collected on a river spawning ground. We then estimated reproductive fitness as the number of offspring (reproductive success) and the number of mates (mating success) using genetic parentage analysis (>5,000 offspring). Sea age is significantly and positively correlated with reproductive and mating success of both sexes whereby older and larger individuals gained the highest reproductive fitness benefits (females: 62.2% increase in offspring/SW and 34.8% increase in mate number/SW; males: 201.9% offspring/SW and 60.3% mates/SW). Younger freshwater age was significantly related to older sea age and thus increased reproductive fitness, but only among females (females: ?33.9% offspring/FW and ?32.4% mates/FW). This result implies that females can obtain higher reproductive fitness by transitioning to the marine environment earlier. In contrast, male mating and reproductive success was unaffected by freshwater age and more males returned at a younger age than females despite the reproductive fitness advantage of later sea age maturation. Our results show that the timing of transitions between juvenile and adult phases has a sex‐specific consequence on female reproductive fitness, demonstrating a life history trade‐off between maturation and reproduction in wild Atlantic salmon.     

Chronic malaria infections increase family inequalities and reduce parental fitness: experimental evidence from a wild bird population

Avian malaria parasites (Plasmodium) occur commonly in wild birds and are an increasingly popular model system for understanding host–parasite co‐evolution. However, whether these parasites have fitness consequences for hosts in endemic areas is much debated, particularly since wild‐caught individuals almost always harbour chronic infections of very low parasite density. We used the anti‐malarial drug Malarone^TM to test experimentally for fitness effects of chronic malaria infection in a wild population of breeding blue tits (Cyanistes caeruleus). Medication caused a pronounced reduction in Plasmodium infection intensity, usually resulting in complete clearance of these parasites from the blood, as revealed by quantitative PCR. Positive effects of medication on malaria‐infected birds were found at multiple stages during breeding, with medicated females showing higher hatching success, provisioning rates and fledging success compared to controls. Most strikingly, we found that treatment of maternal malaria infections strongly altered within‐family differences, with reduced inequality in hatching probability and fledging mass within broods reared by medicated females. These within‐brood effects appear to explain higher fledging success among medicated females and are consistent with a model of parental optimism in which smaller (marginal) offspring can be successfully raised to independence if additional resources become available during the breeding attempt. Overall, these results demonstrate that chronic avian malaria infections, far from being benign, can have significant effects on host fitness and may thus constitute an important selection pressure in wild bird populations.     

Correlates of reproductive success in a wild population of Hippocampus whitei

An analysis of 27 broods born in situ to wild male seahorses Hippocampus whitei , with known partners, showed that female size was the key determinant of the number of young released by the male. There was also an apparent decline in both the number of young per brood, and the size of those young, over the breeding season. The size of the brood and of the young may be more proximate indicators of reproductive success in seahorses than in other fishes, because they can be measured at the time of release, here 20–22 days after fertilization, after which survival is presumed to be relatively higher than in other species. The best model, however, explained <40% of the brood size.     

Hybridization rapidly reduces fitness of a native trout in the wild

Human-mediated hybridization is a leading cause of biodiversity loss worldwide. How hybridization affects fitness and what level of hybridization is permissible pose difficult conservation questions with little empirical information to guide policy and management decisions. This is particularly true for salmonids, where widespread introgression among non-native and native taxa has often created hybrid swarms over extensive geographical areas resulting in genomic extinction. Here, we used parentage analysis with multilocus microsatellite markers to measure how varying levels of genetic introgression with non-native rainbow trout (Oncorhynchus mykiss) affect reproductive success (number of offspring per adult) of native westslope cutthroat trout (Oncorhynchus clarkii lewisi) in the wild. Small amounts of hybridization markedly reduced fitness of male and female trout, with reproductive success sharply declining by approximately 50 per cent, with only 20 per cent admixture. Despite apparent fitness costs, our data suggest that hybridization may spread due to relatively high reproductive success of first-generation hybrids and high reproductive success of a few males with high levels of admixture. This outbreeding depression suggests that even low levels of admixture may have negative effects on fitness in the wild and that policies protecting hybridized populations may need reconsideration.     

The short‐ and long‐term fitness consequences of natal dispersal in a wild bird population

Dispersal is a key process in population and evolutionary ecology. Individual decisions are affected by fitness consequences of dispersal, but these are difficult to measure in wild populations. A long‐term dataset on a geographically closed bird population, the Mauritius kestrel, offers a rare opportunity to explore fitness consequences. Females dispersed further when the availability of local breeding sites was limited, whereas male dispersal correlated with phenotypic traits. Female but not male fitness was lower when they dispersed longer distances compared to settling close to home. These results suggest a cost of dispersal in females. We found evidence of both short‐ and long‐term fitness consequences of natal dispersal in females, including reduced fecundity in early life and more rapid aging in later life. Taken together, our results indicate that dispersal in early life might shape life history strategies in wild populations.     

Sexual selection has minimal impact on effective population sizes in species with high rates of random offspring mortality: An empirical demonstration using fitness distributions

The effective population size (N_e) is a fundamental parameter in population genetics that influences the rate of loss of genetic diversity. Sexual selection has the potential to reduce N_e by causing the sex‐specific distributions of individuals that successfully reproduce to diverge. To empirically estimate the effect of sexual selection on N_e, we obtained fitness distributions for males and females from an outbred, laboratory‐adapted population of Drosophila melanogaster. We observed strong sexual selection in this population (the variance in male reproductive success was ～14 times higher than that for females), but found that sexual selection had only a modest effect on N_e, which was 75% of the census size. This occurs because the substantial random offspring mortality in this population diminishes the effects of sexual selection on N_e, a result that necessarily applies to other high fecundity species. The inclusion of this random offspring mortality creates a scaling effect that reduces the variance/mean ratios for male and female reproductive success and causes them to converge. Our results demonstrate that measuring reproductive success without considering offspring mortality can underestimate N_e and overestimate the genetic consequences of sexual selection. Similarly, comparing genetic diversity among different genomic components may fail to detect strong sexual selection.     

Strong male/male competition allows for nonchoosy females: high levels of polygynandry in a territorial frog with paternal care

Our knowledge about genetic mating systems and the underlying causes for and consequences of variation in reproductive success has substantially improved in recent years. When linked to longitudinal population studies, cross-generational pedigrees across wild populations can help answer a wide suite of questions in ecology and evolutionary biology. We used microsatellite markers and exhaustive sampling of two successive adult generations to obtain population-wide estimates of individual reproductive output of males and females in a natural population of the Neotropical frog Allobates femoralis (Aromobatidae), a pan-Amazonian species that features prolonged iteroparous breeding, male territoriality and male parental care. Parentage analysis revealed a polygynandrous mating system in which high proportions of males (35.5%) and females (56.0%) produced progeny that survived until adulthood. Despite contrasting reproductive strategies, successfully reproducing males and females had similar numbers of mating partners that sired the adult progeny (both sexes: median 2; range 1-6); the numbers of their offspring that reached adulthood were also similar (both sexes: median 2; range 1-8). Measures of reproductive skew indicate selection on males only for their opportunity to breed. Reproductive success was significantly higher in territorial than in nonterritorial males, but unrelated to territory size in males or to body size in both sexes. We hypothesize that female polyandry in this species has evolved because of enhanced offspring survival when paternal care is allocated to multiple partners.     

Upstream migratory behaviour of wild and ranched Atlantic salmon Salmo salar at a natural obstacle in a coastal spate river

The upstream migratory behaviour of wild and ranched Atlantic salmon Salmo salar in a small Irish coastal spate river was investigated using acoustic telemetry. Prespawning migratory behaviour was investigated including movement patterns at a large natural waterfall in the lower reaches of the river. A strong diurnal pattern was observed for upstream migrants at the waterfall indicative of the need for daylight to ascend this complex natural obstacle to migration. Successful passage of the waterfall was also associated with distinct environmental conditions and no difference in migratory ability was detected between wild and ranched origin S. salar. Wild S. salar tended to exhibit a non‐erratic, stepwise upstream migration pattern after ascending the waterfall while ranched S. salar had an increased probability of displaying more erratic migratory behaviour. Wild S. salar penetrated further into the river catchment than ranched S. salar, although male ranched S. salar exhibited the greatest cumulative distance moved prior to the spawning period. The management implications of escaped or released ranched S. salar and movement at natural obstacles are discussed.     

Effects of re‐breeding rates on population size estimation of biennial breeders: results from a model based on albatrosses

Estimating total breeding populations (I) for species that exhibit biennial breeding is generally done from counts of individuals that breed in each year (N), but can be complicated by the fact that the proportion of individuals breeding varies from year to year. Partly, this reflects the proportion of individuals that re‐breed in successive years (re‐breeding rate, p), which is largely, although not exclusively, governed by reproductive failure. Here we show that variation in counts of breeding individuals not only reflects changes in total breeding population but can be sensitive to and powerfully driven by variation in p. A simulation of annual field counts of a bird exhibiting biennial breeding was constructed to explore the effect of re‐breeding attempts on estimations of the total breeding population. The model was used to simulate the consequences of adult mortality and different annual patterns of nesting failures on total breeding population estimates, and to explore the consequences of variation in p on N, when total breeding population remains constant. N is shown to be very sensitive to variations in p, so that even short‐term fluctuations in p can cause changes in N that oscillate for many years ahead. We compare our modelled results with real data for Grey‐headed Albatrosses Thalassarche chrysostoma and demonstrate that, when I is held constant in the model, actual counts may be simulated by variations in p only. Normally, I is unknown and is extrapolated from N on the assumption that N mirrors changes in the size of the total population. Consequently, applying average values of p can result in misleading estimates of total breeding population. We recommend that annual counts of breeding individuals are supplemented with annual estimates of p. Field protocols that aim to estimate annual breeding population size from counts of breeding individuals should be complemented by independent measures of rates of re‐breeding and nest failure.     

Male mating success, reproductive success and multiple paternity in a natural population of sand lizards: behavioural and molecular genetics data

Sand lizard Lacerta agilis females characteristically mate with several males which, in staged mating experiments, results in multiple paternity of the offspring. In order to investigate multiple paternity in a natural population and interpret male reproductive behaviours in terms of sired young, we sampled the blood of females, potential fathers and hatchlings, and determined paternity using multilocus DNA fingerprinting as well as the variation at a single locus detected by the probe (TC) _n . The paternity analyses were preceded by a laboratory experiment in which we established that the parental alleles identified by the single locus probe were inherited in a Mendelian way. Our molecular data demonstrated that 12 out of 13 males (92%) that sired offspring were correctly identified from the 56 sexually mature males in the population. Also smaller males were accepted as sexual partners by the females, but sired fewer young in competition with larger males and were less able to maintain prolonged post-copulatory mate guarding. This may result in that some sexually successful males are only observed inside a female's home range, but never in pair-association with the female.     

The effects of a rust infection on fitness components in a natural population of Tolumnia variegata (Orchidaceae)

The effects of a rust infection (Sphenosphora saphena, Basidiomycetes) on several fitness components of the orchid Tolumnia (Oncidium) variegata were quantified in a subtropical moist forest of Puerto Rico. Infected and uninfected plants of two size categories were observed and manipulated by increasing natural levels of fruit production to determine the effects of infection on short and long-term sexual reproduction, subsequent vegetative and reproductive growth, and mortality. Under artificially high levels of fruit production, infection had no effect on short or long-term reproduction through male or female function except for a modest decline in seed viability in small plants. Under natural levels of fruit production, infection was only related to a reduction in the number of leaves per shoot. At artificially high levels of fruit production, infection reduced leaf length, leaf width, and the number of live shoots. Survival was not associated with rust occurrence. The rust appears to have minor ecological impact on this orchid population.