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).     

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.     

Estimating the proportion of offspring attributable to candidate adults

Statistical methods for estimating genetic parentage are increasingly applied to accommodate limited marker polymorphism and the incomplete sampling of individuals. Neff et al. (2000a, Mol. Ecol. 9, 515–528; 2000b, Mol. Ecol. 9, 529–539) published a method (Pat) that estimates the proportion of next-generation individuals sired by a focal male, taking into account that the male may be genetically compatible, by random chance, with offspring that are not his own. Here we employ this method to reestimate paternity of 68 nest-guarding males from several fish species. The difference between the conventional exclusion-based estimate and Pat was >0.05 in only four of the 68 (5.9%) fish nests analyzed. An analytical formula shows that the difference between the two estimates is expected to be negligible if the focal male is consistent with a large proportion of the genotyped offspring, or if marker polymorphism is high. In addition, computer simulations illustrate how numbers of marker loci and their levels of genetic polymorphism, as well as the mating system of the organism under study, can influence estimates of paternity derived from exclusion-based estimates and Pat. Finally, we discuss various applications of these estimators including cases where additional biological information is present in the form of behavioral observations on parental care.     

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.     

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.     

NMπ 2.0: Software update to minimize the risk of false positives among determinants of reproductive success

In plant populations, parentage analysis helps understand factors shaping individual reproductive success. However, estimating reproductive success determinants based on parentage counts requires decoupling the effects of individual fecundity and propagule dispersal. The neighbourhood model implemented in the NMπ software provides a standard solution for this problem based on the fixed-effects regression-like approach. Nonetheless, it has been recently shown that the method is prone to false discoveries when important fecundity determinants are omitted. To account for the unexplained variance in fecundity, the Bayesian approach was developed based on the new model (the hierarchical neighbourhood model; HNM). Here, I present the NMπ software update that allows the HNM approach to be used in the framework of a friendly interface. More importantly, the HNM approach is now made available for both dispersed (seedlings) and nondispersed (seeds with known mothers) progeny data. The Bayesian approach, among others, selects significant fecundity determinants, estimates the proportion of variance in reproductive potential explained by selected determinants (R²), and provides individual female and male fecundity values. Although the software was designed to handle microsatellite marker data, a solution is proposed for large sets of single nucleotide polymorphisms. The program can be run on Windows (using either a terminal or a graphical interface) as well as (using a terminal) on Linux, or macOS platforms. In any case, NMπ can utilize multicore processors to speed up the analysis. The updated package containing the code, the executable file, the user manual, and example data is available at https://www.ukw.edu.pl/pracownicy/plik/igor_chybicki/3694/ .     

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.     

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.     

Who are the missing parents? Grandparentage analysis identifies multiple sources of gene flow into a wild population

In order to increase the size of declining salmonid populations, supplementation programmes intentionally release fish raised in hatcheries into the wild. Because hatchery-born fish often have lower fitness than wild-born fish, estimating rates of gene flow from hatcheries into wild populations is essential for predicting the fitness cost to wild populations. Steelhead trout (Oncorhynchus mykiss) have both freshwater resident and anadromous (ocean-going) life history forms, known as rainbow trout and steelhead, respectively. Juvenile hatchery steelhead that 'residualize' (become residents rather than go to sea as intended) provide a previously unmeasured route for gene flow from hatchery into wild populations. We apply a combination of parentage and grandparentage methods to a three-generation pedigree of steelhead from the Hood River, Oregon, to identify the missing parents of anadromous fish. For fish with only one anadromous parent, 83% were identified as having a resident father while 17% were identified as having a resident mother. Additionally, we documented that resident hatchery males produced more offspring with wild anadromous females than with hatchery anadromous females. One explanation is the high fitness cost associated with matings between two hatchery fish. After accounting for all of the possible matings involving steelhead, we find that only 1% of steelhead genes come from residualized hatchery fish, while 20% of steelhead genes come from wild residents. A further 23% of anadromous steelhead genes come from matings between two resident parents. If these matings mirror the proportion of matings between residualized hatchery fish and anadromous partners, then closer to 40% of all steelhead genes come from wild trout each generation. These results suggest that wild resident fish contribute substantially to endangered steelhead 'populations' and highlight the need for conservation and management efforts to fully account for interconnected Oncorhynchus mykiss life histories.     

Behavioral and environmental determinants of reproductive success in traditional Moroccan Berber groups

The reproductive histories of women aged 45–70 years from a homogeneous Berber population of South Morocco were sampled from three contrasting environments: a small town (n = 75), villages in the lowlands (n = 217), and villages in the highlands (n = 128). The main reproductive variables oppose the relatively better conditions of fertile life in the lowlands to the more hostile ones in the highlands. Path analysis confirms this difference through reproductive behaviors and suggests the existence of mechanisms for controlling family size in town and in the rural lowlands, but not in the highlands. The estimates of survival function show significant differences among the three groups, the conditions for survival in the highlands being clearly less favorable. Rank tests of the association of survival data with several covariates indicate the association of survival data with vaccinations and with conditions of delivery. In spite of the lower rate of offspring survival, the highlander group would demonstrate a higher overall number of children reaching reproductive maturity, thanks to an extended reproductive span. © 1996 Wiley-Liss, Inc.