Quantification and reduction of bias from sampling larvae to infer population and landscape genetic structure

A well-designed sampling scheme is critical for obtaining accurate results from population genetic studies. Larval samples contain only the genetic material of successful breeders, often of a single year, and may be biased towards particular families. To quantify the bias of using larval samples to infer population and landscape genetic structure and explore how this bias may be reduced using sibship analysis, we analysed eight microsatellite loci from 484 tissue samples of larvae and adults of Columbia spotted frogs (Rana luteiventris) and long-toed salamanders (Ambystoma macrodactylum) at nine breeding sites in north Idaho. Differences in allele frequencies between adult and larval samples were not detected after full-siblings were removed from the larval data set for Columbia spotted frogs; for long-toed salamanders, these differences remained at two out of four ponds. Data from Columbia spotted frog larvae indicated higher levels of differentiation among populations (median difference in F_ST = 0.020, P < 0.01), as predicted by population genetic theory, whereas data from larval samples of long-toed salamanders showed some evidence of lower levels of differentiation among populations (median difference in F_ST = 0.012, P = 0.06). For both species, removing all but one individual from each full-sibling family led to parameter estimates that were closer to those calculated from adult samples for both population and landscape genetic measures. Removal of full-siblings is likely to improve estimates of population genetic parameters; however, knowledge of the species’ breeding system is essential for understanding additional sources of bias when inferring population genetic structure from larval samples.     

The significance of relatedness and gene flow on population genetic structure in the subsocial spider Eresus cinnaberinus (Araneae: Eresidae)

Interdemic selection, inbreeding and highly structured populations have been invoked to explain the evolution of cooperative social behaviour in the otherwise solitary and cannibalistic spiders. The family Eresidae consists of species ranging from solitary and intermediate subsocial to species exhibiting fully cooperative social behaviour. In this study we, in a hierarchical analysis, investigated relatedness of putative family clusters, inbreeding and population genetic structure of the subsocial spider Eresus cinnaberinus. Five hierarchical levels of investigation ranging from large scale genetic structure (distances of 250 and 50 km level 1 and 2) over microgeographic structure (20 km² and 4 km², level 3 and 4) to a single hill transect of 200 m (level 5) were performed. The purpose of level 5 was two-fold: (1) to investigate the relatedness of putative family groups, and (2) to evaluate the influence of both family living and sampling design on higher level estimates. Relatedness estimates of putative family groups showed an average relatedness of R=0.26. There was no indication of inbreeding. In contrast to social spiders, genetic variation was abundant, H_e?0.10. The population genetic structure was intermediate between social and asocial spiders. Genetic variance increased continually across hierarchical levels. Family structured neighbourhoods biased differentiation estimates among level 5 samples (F_ST? 0.04) and level 3 and 4 samples (0.07ST<0.18), and apparent inbreeding among level 3 and 4 samples, F_IS>0, was caused by disjunct sampling from separate neighbourhoods. Larger scale samples were highly differentiated 0.12ST<0.26, depending on level and sampling design. Due to a distance effect family living did not influence estimates of the higher level 1. Although the dispersing sex among social spiders and the subsocial E. cinnebarinus differ, females versus males, female behaviour of both sociality classes lead to high genetic variance.     

Coalescence Times and FST Under a Skewed Offspring Distribution Among Individuals in a Population

Estimates of gene flow between subpopulations based on F_ST (or N_ST) are shown to be confounded by the reproduction parameters of a model of skewed offspring distribution. Genetic evidence of population subdivision can be observed even when gene flow is very high, if the offspring distribution is skewed. A skewed offspring distribution arises when individuals can have very many offspring with some probability. This leads to high probability of identity by descent within subpopulations and results in genetic heterogeneity between subpopulations even when Nm is very large. Thus, we consider a limiting model in which the rates of coalescence and migration can be much higher than for a Wright–Fisher population. We derive the densities of pairwise coalescence times and expressions for F_ST and other statistics under both the finite island model and a many-demes limit model. The results can explain the observed genetic heterogeneity among subpopulations of certain marine organisms despite substantial gene flow.     

A Bayesian method for the joint estimation of outcrossing rate and inbreeding depression

The population outcrossing rate (t) and adult inbreeding coefficient (F) are key parameters in mating system evolution. The magnitude of inbreeding depression as expressed in the field can be estimated given t and F via the method of Ritland (1990). For a given total sample size, the optimal design for the joint estimation of t and F requires sampling large numbers of families (100–400) with fewer offspring (1–4) per family. Unfortunately, the standard inference procedure (MLTR) yields significantly biased estimates for t and F when family sizes are small and maternal genotypes are unknown (a common occurrence when sampling natural populations). Here, we present a Bayesian method implemented in the program BORICE (Bayesian Outcrossing Rate and Inbreeding Coefficient Estimation) that effectively estimates t and F when family sizes are small and maternal genotype information is lacking. BORICE should enable wider use of the Ritland approach for field-based estimates of inbreeding depression. As proof of concept, we estimate t and F in a natural population of Mimulus guttatus. In addition, we describe how individual maternal inbreeding histories inferred by BORICE may prove useful in studies of inbreeding and its consequences.     

Considering sampling bias in close‐kin mark–recapture abundance estimates of Atlantic salmon

Genetic methods for the estimation of population size can be powerful alternatives to conventional methods. Close‐kin mark–recapture (CKMR) is based on the principles of conventional mark–recapture, but instead of being physically marked, individuals are marked through their close kin. The aim of this study was to evaluate the potential of CKMR for the estimation of spawner abundance in Atlantic salmon and how age, sex, spatial, and temporal sampling bias may affect CKMR estimates. Spawner abundance in a wild population was estimated from genetic samples of adults returning in 2018 and of their potential offspring collected in 2019. Adult samples were obtained in two ways. First, adults were sampled and released alive in the breeding habitat during spawning surveys. Second, genetic samples were collected from out‐migrating smolts PIT‐tagged in 2017 and registered when returning as adults in 2018. CKMR estimates based on adult samples collected during spawning surveys were somewhat higher than conventional counts. Uncertainty was small (CV < 0.15), due to the detection of a high number of parent–offspring pairs. Sampling of adults was age‐ and size‐biased and correction for those biases resulted in moderate changes in the CKMR estimate. Juvenile dispersal was limited, but spatially balanced sampling of adults rendered CKMR estimates robust to spatially biased sampling of juveniles. CKMR estimates based on returning PIT‐tagged adults were approximately twice as high as estimates based on samples collected during spawning surveys. We suggest that estimates based on PIT‐tagged fish reflect the total abundance of adults entering the river, while estimates based on samples collected during spawning surveys reflect the abundance of adults present in the breeding habitat at the time of spawning. Our study showed that CKMR can be used to estimate spawner abundance in Atlantic salmon, with a moderate sampling effort, but a carefully designed sampling regime is required.     

Reproductive and Neurobehavioral Effects of Clothianidin Administered to Mice in the Diet

Clothianidin was given in the diet to provide levels of 0% (control), 0.003%, 0.006%, and 0.012% from 5 weeks of age of the F₀ generation to 11 weeks of age of the F₁ generation in mice. Selected reproductive and neurobehavioral parameters were measured. In exploratory behavior in the F₀ generation, average time of movement, number of rearing, and rearing time of adult males increased significantly in a dose‐related manner. There was no adverse effect of clothianidin on litter size, litter weight, or sex ratio at birth. The average body weight of male and female offspring was increased significantly in a dose‐related manner during the early lactation period. With respect to behavioral developmental parameters, swimming head angle at postnatal day (PND) 7 of male offspring was accelerated significantly in a dose‐related manner. Negative geotaxis at PND 7 of female offspring was accelerated significantly in a dose‐related manner. For movement activity of exploratory behavior in the F₁ generation, number of rearing of female offspring increased significantly in a dose‐related manner. Movement time of adult males increased significantly in a dose‐related manner. The dose levels of clothianidin in the present study produced several adverse effects in neurobehavioral parameters in mice. Nevertheless, it would appear that the levels of the actual dietary intake of clothianidin are unlikely to produce adverse effects in humans.     

Statewide and local recruitment of mourning doves in Missouri

Intensive harvests have the potential to greatly affect local mourning dove (Zenaida macroura) populations, a popular gamebird and songbird. To evaluate if recruitment was commensurate with harvest, we applied a ratio-based method to estimate local and statewide mourning dove recruitment across 7 public hunting areas in Missouri from 2005 to 2011. We estimated recruitment from preharvest adult sex ratios and harvest age ratios that incorporated various methods to address potential inherent biases (e.g., bias in the adults of unknown sex in preharvest samples, bias in unknown age wings, and local differential vulnerability; DV). Data from 356 radio-marked doves revealed a DV rate, where hatch year doves were, on average 2.7× more likely to be harvested than adult doves. Recruitment estimates for local areas were highly variable and in some cases, biologically unrealistic (e.g., >10 offspring/female), because of small preharvest sample sizes. However, data pooled statewide provided recruitment estimates of 3.1 offspring/female (±0.3 SE) or 4.1 offspring/female (±0.3 SE), assuming samples of unknown sex doves were female biased or male biased, respectively. Although statewide estimates agree with directly observed rates, the sex ratios and differential vulnerability comprising them vary considerably from what has been previously assumed. Whether preharvest sex ratios are biased from trapping methods has 2 important implications; either regional approaches have overestimated recruitment or the number of females in Missouri's population is much less than originally thought. Because each of these scenarios are important to understanding the effects of regional harvest management on Missouri's dove population, they highlight the importance of a better understanding of biases involved in estimating recruitment. © 2012 The Wildlife Society.     

POSTZYGOTIC ISOLATION OVER MULTIPLE GENERATIONS OF HYBRID DESCENDENTS IN A NATURAL HYBRID ZONE: HOW WELL DO SINGLE‐GENERATION ESTIMATES REFLECT REPRODUCTIVE ISOLATION?

Understanding speciation depends on an accurate assessment of the reproductive barriers separating newly diverged populations. In several taxonomic groups, prezygotic barriers, especially preferences for conspecific mates, are thought to play the dominant role in speciation. However, the importance of postzygotic barriers (i.e., low fitness of hybrid offspring) may be widely underestimated. In this study, we examined how well the widely used proxy of postzygotic isolation (reproductive output of F₁ hybrids) reflects the long‐term fitness consequences of hybridization between two closely related species of birds. Using 40 species‐specific single nucleotide polymorphism (SNP) markers, we genotyped a mixed population of collared and pied flycatchers (Ficedula albicollis and F. hypoleuca) to identify grand‐ and great grand‐offspring from interspecific crosses to derive an accurate, multigeneration estimate of postzygotic isolation. Two independent estimates of fitness show that hybridization results in 2.4% and 2.7% of the number of descendents typical of conspecific pairing. This postzygotic isolation was considerably stronger than estimates based on F₁ hybrids. Our results demonstrate that, in nature, combined selection against hybrids and backcrossed individuals may result in almost complete postzygotic isolation between two comparatively young species. If these findings are general, postzygotic barriers separating hybridizing populations may be much stronger than previously thought.     

A Beta-mixture model for assessing genetic population structure

Summary An important fraction of recently generated molecular data is dominant markers. They contain substantial information about genetic variation but dominance makes it impossible to apply standard techniques to calculate measures of genetic differentiation, such as F‐statistics. In this article, we propose a new Bayesian beta‐mixture model that more accurately describes the genetic structure from dominant markers and estimates multiple F_ST s from the sample. The model also has important application for codominant markers and single‐nucleotide polymorphism (SNP) data. The number of F_ST is assumed unknown beforehand and follows a random distribution. The reversible jump algorithm is used to estimate the unknown number of multiple F_ST s. We evaluate the performance of three split proposals and the overall performance of the proposed model based on simulated dominant marker data. The model could reliably identify and estimate a spectrum of degrees of genetic differentiation present in multiple loci. The estimates of F_ST s also incorporate uncertainty about the magnitude of within‐population inbreeding coefficient. We illustrate the method with two examples, one using dominant marker data from a rare orchid and the other using codominant marker data from human populations.     

ANNUAL DIFFERENCES IN FEMALE REPRODUCTIVE SUCCESS AFFECT SPATIAL AND COHORT-SPECIFIC GENOTYPIC HETEROGENEITY IN PAINTED TURTLES

Long-term ecological data were used to evaluate the relative importance of movements, breeding structure, and reproductive ecological factors to the degree of spatial and age-specific variation in genetic characteristics of painted turtles (Chrysemys picta) on the E. S. George Reserve in southeastern Michigan. Estimates of the degree of spatial genetic structuring were based on the proportion of total genotypic variance partitioned within and between subpopulations (inferred from hierarchical F-statistics based on variation at 18 protein loci), and in terms of gene correlations (co-ancestry among individuals derived from reproductive data on full-sib families of females nesting at specific nesting areas). Little variation in allele frequency was observed among turtles from different marshes (F_mt = 0.003), though significant variation was observed among turtles from different nesting areas associated with each marsh (F_nm = 0.046). Gene correlations among individuals within nesting areas varied greatly over years (0.032-0.171; mean = 0.069) and were negatively correlated to the proportion of females that successfully nested during each year. General concordance between independent estimates of genotypic correlations (i.e., F_nm derived from protein electrophoretic variation vs. mean co-ancestry) suggests that allozyme data, when collected over spatial scales consistent with species behavioral characteristics and reproductive ecology, may accurately reflect the apportionment of gene diversity within and among subpopulations. The magnitude and patterning of allelic variation among nesting areas and individuals appears to be primarily a function of gametic correlations among members of full-sib families, irrespective of the degree of gene flow or female nesting-site fidelity. Comparisons of genetic characteristics among 11 cohorts (1974-1984) revealed that heterozygosity (H) and inbreeding coefficients (F) varied greatly. Cohort estimates of H and F were correlated to female nesting success and to estimates of co-ancestry for the same years. Results clearly reflect the concomitant importance of ecological factors (principally the proportion of the female population that successfully produce offspring during each year) in determining the magnitude and patterning of gene correlations within and among groups, and to the genotypic composition of offspring born during each year.     

Nuclear and chloroplast microsatellite analysis of Abies sachalinensis regeneration on fallen logs in a subboreal forest in Hokkaido, Japan

Fallen logs are the main regeneration sites for Abies sachalinensis (Sachalin fir) in subboreal forests in Japan. We surveyed the spatial genetic structure of different demographic stages in a 4.29-ha natural population of A. sachalinensis . Genetic structure was significant at short distances throughout all stages in this wind-dispersed conifer. To evaluate the effects of fallen-log-dependent recruitment on demography and spatial genetic structure, we conducted parentage analysis of offspring with highly polymorphic nuclear simple sequence repeat and chloroplast simple sequence repeat markers, and developed a new hierarchical Bayesian model to estimate the effects of mother trees and fallen logs on seed dispersal and offspring recruitment. Combined application of nuclear and chloroplast simple sequence repeat markers allowed us to unambiguously identify mother trees of most offspring (> 90%). Female reproductive success was extremely skewed; a few adults produced most of the offspring on fallen logs. Limited distance of effective dispersal and recruitment was seen in the parentage analysis and modelling estimation. These recruitment characters of A. sachalinensis , with a fallen-log-dependent recruitment process, may result in significant genetic structure in early demographic stages.     

A COMPARISON OF THREE INDIRECT METHODS FOR ESTIMATING AVERAGE LEVELS OF GENE FLOW

Three methods for estimating the average level of gene flow in natural population are discussed and compared. The three methods are F_ST, rare alleles, and maximum likelihood. All three methods yield estimates of the combination of parameters (the number of migrants [Nm] in a demic model or the neighborhood size [4πDσ²] in a continuum model) that determines the relative importance of gene flow and genetic drift. We review the theory underlying these methods and derive new analytic results for the expectation of F_ST in stepping-stone and continuum models when small sets of samples are taken. We also compare the effectiveness of the different methods using a variety of simulated data. We found that the F_ST and rare-alleles methods yield comparable estimates under a wide variety of conditions when the population being sampled is demographically stable. They are roughly equally sensitive to selection and to variation in population structure, and they approach their equilibrium values at approximately the same rate. We found that two different maximum-likelihood methods tend to yield biased estimates when relatively small numbers of locations are sampled but more accurate estimates when larger numbers are sampled. Our conclusion is that, although F_ST and rare-alleles methods are expected to be equally effective in analyzing ideal data, practical problems in estimating the frequencies of rare alleles in electrophoretic studies suggest that F_ST is likely to be more useful under realistic conditions.     

Estimating differential reproductive success from nests of related individuals, with application to a study of the mottled sculpin, Cottus bairdi

Understanding how variation in reproductive success is related to demography is a critical component in understanding the life history of an organism. Parentage analysis using molecular markers can be used to estimate the reproductive success of different groups of individuals in natural populations. Previous models have been developed for cases where offspring are random samples from the population but these models do not account for the presence of full- and half-sibs commonly found in large clutches of many organisms. Here we develop a model for comparing reproductive success among different groups of individuals that explicitly incorporates within-nest relatedness. Inference for the parameters of the model is done in a Bayesian framework, where we sample from the joint posterior of parental assignments and fertility parameters. We use computer simulations to determine how well our model recovers known parameters and investigate how various data collection scenarios (varying the number of nests or the number of offspring) affect the estimates. We then apply our model to compare reproductive success among different age groups of mottled sculpin, Cottus bairdi, from a natural population. We demonstrate that older adults are more likely to contribute to a nest and that females in the older age groups contribute more eggs to a nest than younger individuals.     

Inference of Potential Genetic Risks Associated with Large-Scale Releases of Red Sea Bream in Kanagawa Prefecture, Japan Based on Nuclear and Mitochondrial DNA Analysis

Since 1978, millions of hatchery-reared red sea bream (Pagrus major) juveniles have been released in Sagami Bay and Tokyo Bay in Kanagawa Prefecture, Japan. The stock enhancement program has contributed to total catch; however, no information regarding the genetic interactions with wild counterparts is available. Here, we combined 15 microsatellite loci and mitochondrial D-loop sequencing to characterize the genetic resources of red sea bream in Sagami Bay and Tokyo Bay and to elucidate the potential harmful genetic effects associated with fish releases. Both types of markers evidenced higher levels of genetic diversity in wild samples (SB and TB) compared with offspring before stocking (H07 and H08) as well as a hatchery-released sample recaptured in Sagami Bay (HR). Microsatellite F _ST estimates and Bayesian clustering analysis found significant genetic differences among samples (F _ST?=?0.013–0.054), except for the two wild samples (F _ST?=?0.002) and HR vs. H07 (F _ST?=?0.007). On the other hand, mitochondrial-based Ф _ST suggested haplotypic similarity between SB, H07, and HR. The low effective number of females contributing to the offspring over multiple generations may be responsible for the lack of haplotypic differentiation. Moreover, the putative hatchery origin to three fish (8 %) without deformity in the inter-nostril epidermis was inferred for the first time. Our results showed the usefulness of combining nuclear and mitochondrial markers to elucidate genetic interactions between hatchery-released and wild red sea bream and warned about potential harmful genetic effects should interbreeding takes place.     

Multiple breeders, breeder shifts and inclusive fitness returns in an ant

In social insects, colonies may contain multiple reproductively active queens. This leads to potential conflicts over the apportionment of brood maternity, especially with respect to the production of reproductive offspring. We investigated reproductive partitioning in offspring females (gynes) and workers in the ant Formica fusca, and combined this information with data on the genetic returns gained by workers. Our results provide the first evidence that differential reproductive partitioning among breeders can enhance the inclusive fitness returns for sterile individuals that tend non-descendant offspring. Two aspects of reproductive partitioning contribute to this outcome. First, significantly fewer mother queens contribute to gyne (new reproductive females) than to worker brood, such that relatedness increases from worker to gyne brood. Second, and more importantly, adult workers were significantly more related to the reproductive brood raised by the colony, than to the contemporary worker brood. Thus, the observed breeder shift leads to genetic benefits for the adult workers that tend the brood. Our results also have repercussions for genetic population analyses. Given the observed pattern of reproductive partitioning, estimates of effective population size based on worker and gyne samples are not interchangeable.     

Sex‐biased dispersal and high levels of gene flow among local populations in the argentine boa constrictor,Boa constrictor occidentalis

Abstract The knowledge of dispersal is essential to understand the ecology of any species, since population dynamics, spatial distribution and genetic structure are closely tied to patterns of movement. In this paper we estimate dispersal patterns in natural populations of the endangered snake Boa constrictor occidentalis (Serpentes, Boidae), using allozymes as genetic markers. Blood samples were obtained from a total of 120 adult individuals of nine localities from two areas, Sobremonte and Pocho, in Argentina. Only four out of a total of 24 loci were polymorphic: 6‐Pgdh‐1, Cat‐1, Ldh and Hp. The values of expected and observed mean heterozygosities, the percentage of polymorphic loci and mean number of alleles per locus for each population confirm the low levels of genetic variability in this snake. F_ST and N_em mean values were 0.0089 and 46.1 for Sobremonte and 0.0379 and 7.46 for Pocho, indicating important levels of gene flow. A comparison of F_ST between genders in both areas suggests a male‐biased dispersal, which could be explained by the characteristics of the mating system: males carry out an active mate search of receptive females, and philopatry could be selected in females due to the benefits of the familiarity with the natal area in the use of local resources.     

Polyandry and postcopulatory sexual selection in a wild population

When females mate multiply, postcopulatory sexual selection can occur via sperm competition and cryptic female choice. Although postcopulatory selection has the potential to be a major force in driving evolution, few studies have estimated its strength in natural populations. Likewise, although polyandry is widespread across taxa and is the focus of a growing body of research, estimates of natural female mating rates are still limited in number. Microsatellites can be used to estimate the number of mates represented in females' sperm stores and the number of sires contributing to their offspring, enabling comparisons both of polyandry and of two components of postcopulatory selection: the proportion of males that mate but fail to sire offspring, and the degree of paternity skew among the males that do sire offspring. Here, we estimate the number of mates and sires among wild females in the Hawaiian swordtail cricket Laupala cerasina. We compare these estimates to the actual mating rates and paternity shares we observed in a semi‐natural population. Our results show that postcopulatory sexual selection operates strongly in this species: wild females mated with an average minimum of 3.6 males but used the sperm from only 58% of them. Furthermore, among the males that did sire offspring, paternity was significantly skewed. These patterns were similar to those observed in the field enclosure, where females mated with an average of 5.7 males and used the sperm from 62% of their mates, with paternity significantly skewed among the sires.     

Fragmentation by weirs in a riverine system: A study of genetic variation in time and space among populations of European grayling (Thymallus thymallus) in a Danish river system

Human induced habitat alterations affect the genetic structure of many fish populations. Weirs in particular have caused fragmented populations previously connected by gene-flow. We studied the effects of weirs on the distribution of genetic variation within European grayling (Thymallus thymallus) populations from the Skjern River, Denmark. We compared microsatellite data from DNA extracted from historic scale samples collected 60 years ago with data from contemporary samples. Pairwise multilocus F _ST estimates between all contemporary population samples were significant as well as exact tests for population differentiation. Assignment tests of individuals to a set of baseline samples showed correct assignment to the population of origin of between 54 and 79%. Assignment of individuals from recent samples to the historic population samples showed highly variable results (3–83%) of correct assignment suggesting different population histories. Pairwise multilocus F _ST estimates were significantly correlated with the number of intervening weirs but not with waterway distance. A simulation procedure was used to estimate differences in relative population sizes, which indicated that the main river population was approximately three times larger than those of the tributaries. There were no signs of any loss of genetic variation for the river system as a whole during these 60 years. The results show that weirs can be an important factor for creating the current distribution patterns of genetic variation among grayling populations, most likely by only allowing passive downstream drift of fry and obstructing active upstream migration. This revised version was published online in July 2006 with corrections to the Cover Date.     

Modeling the demography of species providing extended parental care: A capture–recapture multievent model with a case study on polar bears (Ursus maritimus)

1. In species providing extended parental care, one or both parents care for altricial young over a period including more than one breeding season. We expect large parental investment and long‐term dependency within family units to cause high variability in life trajectories among individuals with complex consequences at the population level. So far, models for estimating demographic parameters in free‐ranging animal populations mostly ignore extended parental care, thereby limiting our understanding of its consequences on parents and offspring life histories.
2. We designed a capture–recapture multievent model for studying the demography of species providing extended parental care. It handles statistical multiple‐year dependency among individual demographic parameters grouped within family units, variable litter size, and uncertainty on the timing at offspring independence. It allows for the evaluation of trade‐offs among demographic parameters, the influence of past reproductive history on the caring parent''s survival status, breeding probability, and litter size probability, while accounting for imperfect detection of family units. We assess the model performance using simulated data and illustrate its use with a long‐term dataset collected on the Svalbard polar bears (Ursus maritimus).
3. Our model performed well in terms of bias and mean square error and in estimating demographic parameters in all simulated scenarios, both when offspring departure probability from the family unit occurred at a constant rate or varied during the field season depending on the date of capture. For the polar bear case study, we provide estimates of adult and dependent offspring survival rates, breeding probability, and litter size probability. Results showed that the outcome of the previous reproduction influenced breeding probability.
4. Overall, our results show the importance of accounting for i) the multiple‐year statistical dependency within family units, ii) uncertainty on the timing at offspring independence, and iii) past reproductive history of the caring parent. If ignored, estimates obtained for breeding probability, litter size, and survival can be biased. This is of interest in terms of conservation because species providing extended parental care are often long‐living mammals vulnerable or threatened with extinction.