Paternal imprinting of mating preferences between natural populations of house mice (Mus musculus domesticus)

The evolutionary divergence of cues for mate recognition can contribute to early stages of population separation. We compare here two allopatric populations of house mice (Mus musculus domesticus) that have become separated about 3000 years ago. We have used paternity assignments in semi‐natural environments to study the degree of mutual mate recognition according to population origin under conditions of free choice and overlapping generations. Our results provide insights into the divergence of mating cues, but also for the mating system of house mice. We find frequent multiple mating, occurrence of inbreeding and formation of extended family groups. In addition, many animals show strong mate fidelity, that is, frequent choice of the same mating partners in successive breeding cycles, indicating a role for familiarity in mating preference. With respect to population divergence, we find evidence for assortative mating, but only under conditions where the animals had time to familiarize themselves with mating partners from their own population. Most interestingly, the first‐generation offspring born in the enclosure showed a specific mating pattern. Although matings between animals of hybrid population origin with animals of pure population origin should have occurred with equal frequency with respect to matching the paternal or maternal origin, paternal matching with mates from their own populations occurred much more often. Our findings suggest that paternally imprinted cues play a role in mate recognition between mice and that the cues evolve fast, such that animals of populations that are separated since not more than 3000 years can differentially recognize them.     

No evidence for inbreeding avoidance in a great reed warbler population

Inbreeding depression may drive the evolution of inbreedingavoidance through dispersal and mate choice. In birds, manyspecies show female-biased dispersal, which is an effectiveinbreeding avoidance mechanism. In contrast, there is scarceevidence in birds for kin discriminative mate choice, whichmay, at least partly, reflect difficulties detecting it. First,kin discrimination may be realized as dispersal, and this isdifficult to distinguish from other causes of dispersal. Second,even within small, isolated populations, it is often difficultto determine the potential candidates available to a femalewhen choosing a mate. We sought evidence for inbreeding avoidancevia kin discrimination in a breeding population of great reedwarblers (Acrocephalus arundinaceus) studied over 17 years.Inbreeding depression is strong in the population, suggestingthat it would be adaptive to avoid relatives as mates. Detaileddata on timing of settlement and mate search movements madeit possible to identify candidate mates for each female, andlong-term pedigrees and resolved parentage enabled us to estimaterelatedness between females and their candidate mates. We foundno evidence for kin discrimination: mate choice was random withrespect to relatedness when all mate-choice events were considered,and, after correction for multiple tests, also in all breedingyears. We suggest that dispersal is a sufficient inbreedingavoidance mechanism in most situations, although the lack ofkin discriminative mate choice has negative consequences forsome females, because they end up mating with closely relatedmales that lowers their fitness.     

Re‐mating across years and intralineage polygyny are associated with greater than expected levels of inbreeding in wild red deer

The interaction between philopatry and nonrandom mating has important consequences for the genetic structure of populations, influencing co‐ancestry within social groups but also inbreeding. Here, using genetic paternity data, we describe mating patterns in a wild population of red deer (Cervus elaphus) which are associated with marked consequences for co‐ancestry and inbreeding in the population. Around a fifth of females mate with a male with whom they have mated previously, and further, females frequently mate with a male with whom a female relative has also mated (intralineage polygyny). Both of these phenomena occur more than expected under random mating. Using simulations, we demonstrate that temporal and spatial factors, as well as skew in male breeding success, are important in promoting both re‐mating behaviours and intralineage polygyny. However, the information modelled was not sufficient to explain the extent to which these behaviours occurred. We show that re‐mating and intralineage polygyny are associated with increased pairwise relatedness in the population and a rise in average inbreeding coefficients. In particular, the latter resulted from a correlation between male relatedness and rutting location, with related males being more likely to rut in proximity to one another. These patterns, alongside their consequences for the genetic structure of the population, have rarely been documented in wild polygynous mammals, yet they have important implications for our understanding of genetic structure, inbreeding avoidance and dispersal in such systems.     

Banded mongooses avoid inbreeding when mating with members of the same natal group

Inbreeding and inbreeding avoidance are key factors in the evolution of animal societies, influencing dispersal and reproductive strategies which can affect relatedness structure and helping behaviours. In cooperative breeding systems, individuals typically avoid inbreeding through reproductive restraint and/or dispersing to breed outside their natal group. However, where groups contain multiple potential mates of varying relatedness, strategies of kin recognition and mate choice may be favoured. Here, we investigate male mate choice and female control of paternity in the banded mongoose (Mungos mungo), a cooperatively breeding mammal where both sexes are often philopatric and mating between relatives is known to occur. We find evidence suggestive of inbreeding depression in banded mongooses, indicating a benefit to avoiding breeding with relatives. Successfully breeding pairs were less related than expected under random mating, which appeared to be driven by both male choice and female control of paternity. Male banded mongooses actively guard females to gain access to mating opportunities, and this guarding behaviour is preferentially directed towards less closely related females. Guard–female relatedness did not affect the guard's probability of gaining reproductive success. However, where mate‐guards are unsuccessful, they lose paternity to males that are less related to the females than themselves. Together, our results suggest that both sexes of banded mongoose use kin discrimination to avoid inbreeding. Although this strategy appears to be rare among cooperative breeders, it may be more prominent in species where relatedness to potential mates is variable, and/or where opportunities for dispersal and mating outside of the group are limited.     

GENETIC SIMILARITY BETWEEN PARENTS PREDICTS HATCHING FAILURE: NONINCESTUOUS INBREEDING IN THE GREAT REED WARBLER?

The DNA-fingerprinting technique was used to find the true pedigrees and to detect the overall genetic similarity between mates of great reed warblers (Acrocephalus arundinaceus) at an isolated breeding site in Sweden. The study covered 4 yr preceded by 3 yr when almost all adults and nestlings in the study area had been banded. DNA fingerprinting revealed that the putative father had sired 97% of the young (N = 455). The mate's genetic similarity, revealed as the proportion of bands shared in restriction fragment length polymorphism (RFLP) patterns, was high compared with other species of wild birds. Also, band sharing was higher between mates native to the area than between pairs in which the female was experimentally introduced from a distant breeding site. Hatching success of eggs was negatively correlated with the degree of genetic similarity between the mates, whereas pedigree data, up to the level of great-grandparents, clearly demonstrated an absence of close inbreeding. These are the first data showing a significant fitness cost associated with the choice of a mate that has high genetic similarity, even if it is not a close kin. This cost might be caused by generalized negative consequences of genomewide inbreeding in the present study, possibly accentuated by recent population bottlenecks.     

Assessing the reproductive consequences of mate retention and pair bond duration in Thorn-tailed Rayadito (Aphrastura spinicauda), a short-lived,socially monogamous neotropical bird

The adaptive value of mate retention has been studied in several socially monogamous birds but evidence of reproductive benefits for short-lived species is inconclusive. Most studies come from northern latitudes but more research on tropical birds is needed, as these species typically show higher survival rates and longer pair bonds than those from temperate regions. We gathered data on the reproductive biology of a subtropical, isolated population of Thorn-tailed Rayadito Aphrastura spinicaudaduring 2008–2017 to evaluate the reproductive consequences of mate retention. We examined data from 243 breeding attempts made by 159 breeding pairs. We found that ~30% of all breeding pairs bred together during at least two consecutive years, and some were mated for 6 years. The main cause of pair dissolution was mate loss, not divorce. Mixed-effects models provided moderate evidence for positive effects of mate retention and successive remating on reproductive success. Newly formed pairs laid eggs later and had slightly smaller clutches than remated pairs. Furthermore, clutch size seemed to increase with successive remating. Overall, our results suggest that newly formed pairs are less efficient in reproduction and that minor yearly reproductive benefits of mate retention might accumulate for birds that are able to breed with the same partner over many years. Because breeding habitat is limited in our study population, Thorn-tailed Rayaditos could benefit from remating if the number of individuals that can breed exceeds the number of available breeding positions. Profitable long-term pair bonds might be more frequent in tropical birds and therefore more studies are needed to assess the prevalence of remating-mediated effects on reproduction in relatively short-lived monogamous species breeding in tropical regions.     

Genetic variability characterization of the moroccan houbara bustard (Chlamydotis undulata undulata) inferred from pedigree analysis

A Moroccan Houbara Bustard pedigree was analyzed to evaluate the genetic variability in captive breeding population using genealogical approaches. The whole Houbara breeding flock (WP) for the period 1993–2004 was made up of 531 birds comprising 346 females and 185 males. The reference population (RP) comprised 198 individuals ready for reproduction from 2000 to 2004 cohorts. The corresponding percentage of known ancestors was estimated as 98.23% for the parent generation, 41.19% for the grandparent generation and 7.00% for the great grandparents generation. The average generation interval for Houbara was computed as 4.64 years. Genetic variability loss per generation was ascertained using the effective population size (), the founder genome equivalent (fge), the effective number of ancestors and founders (fa) and (fe), respectively, for the RP and across each cohort. The results showed no bottleneck events in the breed but some loss of genetic variability just after the initiation of the conservation program. However, the annual effective population size based on the realized increase in inbreeding () was estimated to be 207 for the RP and 1,000 for the WP. With regard to conservation breeding schemes, the genealogical evidence presented here is very useful as it revealed the positive effect of migration on Houbara breeding. The mating strategies will assist in the future control and management of the genetic variability of this population. Zoo Biol. 32:366‐373, 2013. © 2012 Wiley Periodicals, Inc.     

A novel framework for evaluating in situ breeding management strategies in endangered populations

Conservation breeding management aims to reduce inbreeding and maximize the retention of genetic diversity in endangered populations. However, breeding management of wild populations is still rare, and there is a need for approaches that provide data-driven evidence of the likelihood of success of alternative in situ strategies. Here, we provide an analytical framework that uses in silico simulations to evaluate, for real wild populations, (i) the degree of population-level inbreeding avoidance, (ii) the genetic quality of mating pairs, and (iii) the potential genetic benefits of implementing two breeding management strategies. The proposed strategies aim to improve the genetic quality of breeding pairs by splitting detrimental pairs and allowing the members to re-pair in different ways. We apply the framework to the wild population of the Critically Endangered helmeted honeyeater by combining genomic data and field observations to estimate the inbreeding (i.e., pair-kinship) and genetic quality (i.e., Mate Suitability Index) of all mating pairs for seven consecutive breeding seasons. We found no evidence of population-level inbreeding avoidance and that ~91.6% of breeding pairs were detrimental to the genetic health of the population. Furthermore, the framework revealed that neither proposed management strategy would significantly improve the genetic quality or reduce inbreeding of the mating pairs in this population. Our results demonstrate the usefulness of our analytical framework for testing the efficacy of different in situ breeding management strategies and for making evidence-based management decisions.     

Life history mediates mate limitation and population viability in self‐incompatible plant species

Genetically controlled self‐incompatibility systems represent links between genetic diversity and plant demography with the potential to directly impact on population dynamics. We use an individual‐based spatial simulation to investigate the demographic and genetic consequences of different self‐incompatibility systems for plants that vary in reproductive capacity and lifespan. The results support the idea that, in the absence of inbreeding effects, populations of self‐incompatible species will often be smaller and less viable than self‐compatible species, particularly for shorter‐lived organisms or where potential fecundity is low. At high ovule production and low mortality, self‐incompatible and self‐compatible species are demographically similar, thus self‐incompatibility does not automatically lead to reduced mate availability or population viability. Overall, sporophytic codominant self‐incompatibility was more limiting than gametophytic or sporophytic dominant systems, which generally behaved in a similar fashion. Under a narrow range of conditions, the sporophytic dominant system maintained marginally greater mate availability owing to the production of S locus homozygotes. While self‐incompatibility reduces population size and persistence for a broad range of conditions, the actual number of S alleles, beyond that required for reproduction, is important for only a subset of life histories. For these situations, results suggest that addition of new S alleles may result in significant demographic rescue.     

Inbreeding and inbreeding depression in endangered red wolves (Canis rufus)

In natural populations, the expression and severity of inbreeding depression can vary widely across taxa. Describing processes that influence the extent of inbreeding and inbreeding depression aid in our understanding of the evolutionary history of mating systems such as cooperative breeding and nonrandom mate selection. Such findings also help shape wildlife conservation theory because inbreeding depression reduces the viability of small populations. We evaluated the extent of inbreeding and inbreeding depression in a small, re‐introduced population of red wolves (Canis rufus) in North Carolina. Since red wolves were first re‐introduced in 1987, pedigree inbreeding coefficients (f) increased considerably and almost every wild born wolf was inbred (average f = 0.154 and max f = 0.383). The large inbreeding coefficients were due to both background relatedness associated with few founders and numerous close relative matings. Inbreeding depression was most evident for adult body size and generally absent for direct fitness measures such as reproductive success and survival; no lethal equivalents (LE = 0.00) were detected in juvenile survival. The lack of strong inbreeding depression in direct measures of fitness could be due to a founder effect or because there were no outbred individuals for comparison. Our results highlight the variable expression of inbreeding depression across traits and the need to measure a number of different traits when evaluating inbreeding depression in a wild population.     

Genetic rescue in a severely inbred wolf population

Natural populations are becoming increasingly fragmented which is expected to affect their viability due to inbreeding depression, reduced genetic diversity and increased sensitivity to demographic and environmental stochasticity. In small and highly inbred populations, the introduction of only a few immigrants may increase vital rates significantly. However, very few studies have quantified the long‐term success of immigrants and inbred individuals in natural populations. Following an episode of natural immigration to the isolated, severely inbred Scandinavian wolf (Canis lupus) population, we demonstrate significantly higher pairing and breeding success for offspring to immigrants compared to offspring from native, inbred pairs. We argue that inbreeding depression is the underlying mechanism for the profound difference in breeding success. Highly inbred wolves may have lower survival during natal dispersal as well as competitive disadvantage to find a partner. Our study is one of the first to quantify and compare the reproductive success of first‐generation offspring from migrants vs. native, inbred individuals in a natural population. Indeed, our data demonstrate the profound impact single immigrants can have in small, inbred populations, and represent one of very few documented cases of genetic rescue in a population of large carnivores.     

Loss of genetic variability in social spiders: genetic and phylogenetic consequences of population subdivision and inbreeding

The consequences of population subdivision and inbreeding have been studied in many organisms, particularly in plants. However, most studies focus on the short‐term consequences, such as inbreeding depression. To investigate the consequences of both population fragmentation and inbreeding for genetic variability in the longer term, we here make use of a natural inbreeding experiment in spiders, where sociality and accompanying population subdivision and inbreeding have evolved repeatedly. We use mitochondrial and nuclear data to infer phylogenetic relationships among 170 individuals of Anelosimus spiders representing 23 species. We then compare relative mitochondrial and nuclear genetic variability of the inbred social species and their outbred relatives. We focus on four independently derived social species and four subsocial species, including two outbred–inbred sister species pairs. We find that social species have 50% reduced mitochondrial sequence divergence. As inbreeding is not expected to reduce genetic variability in the maternally inherited mitochondrial genome, this suggests the loss of variation due to strong population subdivision, founder effects, small effective population sizes (colonies as individuals) and lineage turnover. Social species have < 10% of the nuclear genetic variability of the outbred species, also suggesting the loss of genetic variability through founder effects and/or inbreeding. Inbred sociality hence may result in reduction in variability through various processes. Sociality in most Anelosimus species probably arose relatively recently (0.1–2 mya), with even the oldest social lineages having failed to diversify. This is consistent with the hypothesis that inbred spider sociality represents an evolutionary dead end. Heterosis underlies a species potential to respond to environmental change and/or disease. Inbreeding and loss of genetic variability may thus limit diversification in social Anelosimus lineages and similarly pose a threat to many wild populations subject to habitat fragmentation or reduced population sizes.     

High resolution analysis of mating systems: inbreeding in natural populations of Pinus radiata

Pinus radiata has a history of population bottlenecks and is currently restricted to five relatively small populations, three in mainland California, and two on islands off the coast of Baja California. Using highly polymorphic microsatellite markers and a newly developed statistical approach, we were able to estimate individual inbreeding coefficients and can thus analyse the mating system with high resolution. We find a bimodal distribution of inbreeding coefficients: most individuals result from selfing whereas few (in the mainland populations) to a modest number (in the island populations) are likely selfed. In most other pine species and presumably in the ancestral P. radiata population, occurrence of mature selfed individuals would be impossible because of the high genetic load. We therefore conclude that inbreeding depression has been purged in P. radiata and that the mating system has changed as a consequence.     

Environment-dependent selection on mate choice in a natural population of birds

Female mate choice acts as an important evolutionary force, yet the influence of the environment on both its expression and the selective pressures acting upon it remains unknown. We found consistent heritable differences between females in their choice of mate based on ornament size during a 25-year study of a population of collared flycatchers. However, the fitness consequences of mate choice were dependent on environmental conditions experienced whilst breeding. Females breeding with highly ornamented males experienced high relative fitness during dry summer conditions, but low relative fitness during wetter years. Our results imply that sexual selection within a population can be highly variable and dependent upon the prevailing weather conditions experienced by individuals.     

Mate fidelity in a polygamous shorebird,the snowy plover (Charadrius nivosus)

Social monogamy has evolved multiple times and is particularly common in birds. However, it is not well understood why some species live in long‐lasting monogamous partnerships while others change mates between breeding attempts. Here, we investigate mate fidelity in a sequential polygamous shorebird, the snowy plover (Charadrius nivosus), a species in which both males and females may have several breeding attempts within a breeding season with the same or different mates. Using 6 years of data from a well‐monitored population in Bahía de Ceuta, Mexico, we investigated predictors and fitness implications of mate fidelity both within and between years. We show that in order to maximize reproductive success within a season, individuals divorce after successful nesting and re‐mate with the same partner after nest failure. Therefore, divorced plovers, counterintuitively, achieve higher reproductive success than individuals that retain their mate. We also show that different mating decisions between sexes predict different breeding dispersal patterns. Taken together, our findings imply that divorce is an adaptive strategy to improve reproductive success in a stochastic environment. Understanding mate fidelity is important for the evolution of monogamy and polygamy, and these mating behaviors have implications for reproductive success and population productivity.     

Cryptic inbreeding depression in a growing population of a long‐lived species

Genetic effects are often overlooked in endangered species monitoring, and populations showing positive growth are often assumed to be secure. However, the continued reproductive success of a few individuals may mask issues such as inbreeding depression, especially in long‐lived species. Here, we test for inbreeding depression in little spotted kiwi (Apteryx owenii) by comparing a population founded with two birds to one founded with 40 birds, both from the same source population and both showing positive population growth. We used a combination of microsatellite genotypes, nest observations and modelling to examine the consequences of assessing population viability exclusively via population growth. We demonstrate (i) significantly lower hatching success despite significantly higher reproductive effort in the population with two founders; (ii) positive growth in the population with two founders is mainly driven by ongoing chick production of the founding pair; and (iii) a substantial genetic load in the population founded with two birds (10–15 diploid lethal equivalents). Our results illustrate that substantial, cryptic inbreeding depression may still be present when a population is growing, especially in long‐lived species with overlapping generations.     

Malformed offspring,sibling matings,and selection against inbreeding in the sand lizard (Lacerta agilis)

We demonstrated that sand lizards (Lacerta agilis) are more likely to have malformed offspring when they mate with siblings. Offspring with malformations, such as deformed limbs and heads, have zero survival in a natural population. Normal-looking siblings of malformed hatchlings also had a reduced survival in the wild, compared to offspring from clutches in which all siblings appeared normal. The proportion of malformed hatchlings in the natural population was ca. 10%, in spite of differences in juvenile dispersal between males and females. Male juveniles disperse significantly further from their natal sites than do female juveniles.     

Sperm storage reduces the strength of the mate‐finding Allee effect

Mate searching is a key component of sexual reproduction that can have important implications for population viability, especially for the mate‐finding Allee effect. Interannual sperm storage by females may be an adaptation that potentially attenuates mate limitation, but the demographic consequences of this functional trait have not been studied. Our goal is to assess the effect of female sperm storage durability on the strength of the mate‐finding Allee effect and the viability of populations subject to low population density and habitat alteration. We used an individual‐based simulation model that incorporates realistic representations of the demographic and spatial processes of our model species, the spur‐thighed tortoise (Testudo graeca). This allowed for a detailed assessment of reproductive rates, population growth rates, and extinction probabilities. We also studied the relationship between the number of reproductive males and the reproductive rates for scenarios combining different levels of sperm storage durability, initial population density, and landscape alteration. Our results showed that simulated populations parameterized with the field‐observed demographic rates collapsed for short sperm storage durability, but were viable for a durability of one year or longer. In contrast, the simulated populations with a low initial density were only viable in human‐altered landscapes for sperm storage durability of 4 years. We find that sperm storage is an effective mechanism that can reduce the strength of the mate‐finding Allee effect and contribute to the persistence of low‐density populations. Our study highlights the key role of sperm storage in the dynamics of species with limited movement ability to facilitate reproduction in patchy landscapes or during population expansion. This study represents the first quantification of the effect of sperm storage durability on population dynamics in different landscapes and population scenarios.     

The new kid on the block: immigrant males win big whereas females pay fitness cost after dispersal

Dispersal is nearly universal; yet, which sex tends to disperse more and their success thereafter depends on the fitness consequences of dispersal. We asked if lifetime fitness differed between residents and immigrants (successful between‐population dispersers) and their offspring using 29 years of monitoring from North American red squirrels (Tamiasciurus hudsonicus) in Canada. Compared to residents, immigrant females had 23% lower lifetime breeding success (LBS), while immigrant males had 29% higher LBS. Male immigration and female residency were favoured. Offspring born to immigrants had 15–43% lower LBS than offspring born to residents. We conclude that immigration benefitted males, but not females, which appeared to be making the best of a bad lot. Our results are in line with male‐biased dispersal being driven by local mate competition and local resource enhancement, while the intergenerational cost to immigration is a new complication in explaining the drivers of sex‐biased dispersal.     

Testing alternative captive breeding strategies with the subsequent release into the wild

We used the housefly (Musca domestica L.) as an experimental model to compare two strategies for the captive breeding of an endangered species: a strategy to minimize inbreeding and balance founder contributions (termed “MAI” for “maximum avoidance of inbreeding”) versus a scheme to select against less fit individuals (disregarding relatedness). By balancing the initial founder contributions, the MAI protocol was analogous to methods for minimizing kinship. In both breeding strategies, the population growth rate was limited to a maximum increase of 50% per generation. Five replicate populations, each starting with five male–female pairs, were subjected to five generations of captive breeding. Six generations of simulated “release into the wild” allowed ad lib breeding with less restrictive population growth potential, in either a benign or stressful environment (i.e., constant or variable temperature). Population size, fecundity, and fertility were assayed throughout the experiment, with juvenile‐to‐adult survival assayed in the second phase of the project. Allozyme assays determined the resultant inbreeding coefficients from the captive breeding schemes. The MAI breeding scheme resulted in significantly lower inbreeding coefficients and higher fitness, with qualitatively reduced extinction potential, most notable in the stressful environment. Spontaneous fitness rebounds suggested that the MAI strategy facilitated some form of purging of inbreeding depression effects. Importantly, the advantages of the MAI strategy were difficult to detect during the captive breeding phase, suggesting that the long‐term advantages of the MAI approach could be underestimated in actual breeding programs. We concur with the common recommendation of maximum avoidance of inbreeding at least for systems with low reproductive potential. Zoo Biol 0:1–18, 2005. © 2005 Wiley‐Liss, Inc.