Positive assortative mating with selection restrictions on group coancestry enhances gain while conserving genetic diversity in long-term forest tree breeding

Selection and mating principles in a closed breeding population (BP) were studied by computer simulation. The BP was advanced, either by random assortment of mates (RAM), or by positive assortative mating (PAM). Selection was done with high precision using clonal testing. Selection considered both genetic gain and gene diversity by "group-merit selection", i.e. selection for breeding value weighted by group coancestry of the selected individuals. A range of weights on group coancestry was applied during selection to vary parent contributions and thereby adjust the balance between gain and diversity. This resulted in a series of scenarios with low to high effective population sizes measured by status effective number. Production populations (PP) were selected only for gain, as a subset of the BP. PAM improved gain in the PP substantially, by increasing the additive variance (i.e. the gain potential) of the BP. This effect was more pronounced under restricted selection when parent contributions to the next generation were more balanced with within-family selection as the extreme, i.e. when a higher status effective number was maintained in the BP. In that case, the additional gain over the BP mean for the clone PP and seed PPs was 32 and 84% higher, respectively, for PAM than for RAM in generation 5. PAM did not reduce gene diversity of the BP but increased inbreeding, and in that way caused a departure from Hardy-Weinberg equilibrium. The effect of inbreeding was eliminated by recombination during the production of seed orchard progeny. Also, for a given level of inbreeding in the seed orchard progeny or in a mixture of genotypes selected for clonal deployment, gain was higher for PAM than for RAM. After including inbreeding depression in the simulation, inbreeding was counteracted by selection, and the enhancement of PAM on production population gain was slightly reduced. In the presence of inbreeding depression the greatest PP gain was achieved at still higher levels of status effective number, i.e. when more gene diversity was conserved in the BP. Thus, the combination of precise selection and PAM resulted in close to maximal short-term PP gain, while conserving maximal gene diversity in the BP.Communicated by O. Savolainen     

The scale‐of‐choice effect and how estimates of assortative mating in the wild can be biased due to heterogeneous samples

The mode in which sexual organisms choose mates is a key evolutionary process, as it can have a profound impact on fitness and speciation. One way to study mate choice in the wild is by measuring trait correlation between mates. Positive assortative mating is inferred when individuals of a mating pair display traits that are more similar than those expected under random mating while negative assortative mating is the opposite. A recent review of 1134 trait correlations found that positive estimates of assortative mating were more frequent and larger in magnitude than negative estimates. Here, we describe the scale‐of‐choice effect (SCE), which occurs when mate choice exists at a smaller scale than that of the investigator's sampling, while simultaneously the trait is heterogeneously distributed at the true scale‐of‐choice. We demonstrate the SCE by Monte Carlo simulations and estimate it in two organisms showing positive (Littorina saxatilis) and negative (L. fabalis) assortative mating. Our results show that both positive and negative estimates are biased by the SCE by different magnitudes, typically toward positive values. Therefore, the low frequency of negative assortative mating observed in the literature may be due to the SCE's impact on correlation estimates, which demands new experimental evaluation.     

Temporal variation of heterozygosity‐based assortative mating and related benefits in a lesser kestrel population

Heterozygosity as a target of mate choice has received much attention in recent years and there is growing evidence supporting its role in the evolution of mate preferences. In this study we analyse mating patterns in relation to heterozygosity in a lesser kestrel (Falco naumanni) population intensively monitored over six study years (2002–2007). The magnitude of heterozygosity‐based assortative mating varied over time, being particularly patent in the last study years (2006, 2007). We have found evidence that this mating pattern entails both direct and indirect‐genetic benefits. Clutch size increased with female heterozygosity and more heterozygous males raised a higher number of fledglings particularly in those years when the strength of the heterozygosity‐based assortative mating was markedly higher. In the last study year, parent–offspring correlation of heterozygosity was stronger and higher than the expected if individuals would have randomly mated with respect to heterozygosity. Overall, our results offer empirical support to the heterozygous mate hypothesis of sexual selection but suggest that genetic diversity may act as a temporally variable target for mate choice.     

Sampling scale can cause bias in positive assortative mating estimates: evidence from two intertidal snails

Assortative mating in the wild is commonly estimated by correlating between traits in mating pairs (e.g. the size of males and females). Unfortunately, such an approach may suffer from considerable sampling bias when the distribution of different expressions of a trait in the wild is nonrandom (e.g. when segregation of different size classes of individuals occurs in different microhabitats or areas). Consequently, any observed trait correlation in the wild can be an artefact of pooling heterogeneous samples of mating pairs from different microhabitats or areas rather than true nonrandom matings. This bias in estimating trait correlations as a result of sampling scale is termed the scale‐of‐choice effect (SCE). In the present study, we use two intertidal littorinid species from Hong Kong to show how the SCE can bias size‐assortative mating estimates from mating pairs captured in the wild, empirically demonstrating the influence of this effect on measures of positive assortative mating. This finding cautions that studies overlooking the SCE may have misinterpreted the magnitude and the cause of assortative mating, and we provide a new analytical approach for protecting against this potential bias in future studies.     

Emergence and loss of assortative mating in sympatric speciation

We have studied an agent model which presents the emergence of sexual barriers through the onset of assortative mating, a condition that might lead to sympatric speciation. In the model, individuals are characterized by two traits, each determined by a single locus A or B. Heterozygotes on A are penalized by introducing an adaptive difference from homozygotes. Two niches are available. Each A homozygote is adapted to one of the niches. The second trait, called the marker trait has no bearing on the fitness. The model includes mating preferences, which are inherited from the mother and subject to random variations. A parameter controlling recombination probabilities of the two loci is also introduced. We study the phase diagram by means of simulations, in the space of parameters (adaptive difference, carrying capacity, recombination probability). Three phases are found, characterized by (i) assortative mating, (ii) extinction of one of the A alleles and (iii) Hardy-Weinberg like equilibrium. We also make perturbations of these phases to see how robust they are. Assortative mating can be gained or lost with changes that present hysteresis loops, showing the resulting equilibrium to have partial memory of the initial state and that the process of going from a polymorphic panmictic phase to a phase where assortative mating acts as sexual barrier can be described as a first-order transition.     

Sexual size dimorphism and assortative mating in Carolina Wrens

ABSTRACT.   Sexual size dimorphism (SSD) may be due to sexual and natural selection, but identifying specific mechanisms that generate such dimorphism in a species is difficult. I examined SSD in Carolina Wrens ( Thryothorus ludovicianus ) by examining (1) the degree of SSD in the population and between pairs using five morphometrics, (2) assortative mating patterns based on size and age, and (3) relationships between size and longevity. Analysis revealed that males were significantly larger than females in all body measurements. For example, mass, bill, and wing measurements yielded a canonical variable that permitted separation of the sexes and linear classification functions correctly determined the sex of 95% (238/250) of all wrens measured. No evidence was found to suggest that SSD was related to resource partitioning. However, assortative mating trends based on morphometrics (e.g., wing length), positive associations between longevity and morphometrics (e.g., wing length in females and body size in males), and intense male-male contests for territorial resources year-round provide evidence that sexual selection may contribute to SSD in Carolina Wrens.     

Phenotypic divergence but not genetic distance predicts assortative mating among species of a cichlid fish radiation

The hypothesis of ecological divergence giving rise to premating isolation in the face of gene flow is controversial. However, this may be an important mechanism to explain the rapid multiplication of species during adaptive radiation following the colonization of a new environment when geographical barriers to gene flow are largely absent but underutilized niche space is abundant. Using cichlid fish, we tested the prediction of ecological speciation that the strength of premating isolation among species is predicted by phenotypic rather than genetic distance. We conducted mate choice experiments between three closely related, sympatric species of a recent radiation in Lake Mweru (Zambia/DRC) that differ in habitat use and phenotype, and a distantly related population from Lake Bangweulu that resembles one of the species in Lake Mweru. We found significant assortative mating among all closely related, sympatric species that differed phenotypically, but none between the distantly related allopatric populations of more similar phenotype. Phenotypic distance between species was a good predictor of the strength of premating isolation, suggesting that assortative mating can evolve rapidly in association with ecological divergence during adaptive radiation. Our data also reveals that distantly related allopatric populations that have not diverged phenotypically, may hybridize when coming into secondary contact, e.g. upon river capture because of diversion of drainage systems.     

Effect of assortative mating on genetic change due to selection

Summary Two mathematical models (A and B) were used to study joint effects of selection and assortative mating on genetic change. Computer simulation was used to verify and extend the results. In each model, the genotype was additive with equal effects at each of N loci and the environmental distribution was N(0, ²). In Model A, each locus had two alleles; in Model B, allelic effects at each locus followed a normal distribution. Using Model A, genetic change with assortative or random mating of selected parents was evaluated for combinations of number of loci (N = 1, 2, 3), heritability in base population (H^[0] = 0.2, 0.5, 0.8), allelic frequency in base population (p = 0.1, 0.5), and proportion selected ( = 0.20, 0.85). Using Model B, genetic change with or without assortative mating was calculated for combinations of N (1, 2, 3, 5, 10, 100, H^[0] (0.2, 0.5, 0.8) and (0.20, 0.85). Response to selection under both mating systems in a finite population was estimated using Model A from 200 replications of a computer simulation; this was done for all combinations of N (1,2, 3, 5, 10) and (0.20, 0.85), with H^[0] = 0.5 and p = 0.1. Results obtained with both models indicate that the effect of assortative mating on genetic change increases with H^[0] and , and decreases with p. With Model A, the relationship between N and the effect of assortative mating on genetic change was not clear; with Model B, however, the advantage of assortative over random mating increased with N, as expected. Simulation results were in agreement with theory of Model A. This study indicates that selection with assortative mating can have a sizable (10 to 20%) long-term advantage over selection with random mating of parents when H^[0] is high, p is low and is large.     

Incipient allochronic speciation due to non-selective assortative mating by flowering time, mutation and genetic drift

We model the evolution of flowering time using a multilocus quantitative genetic model with non-selective assortative mating and mutation to investigate incipient allochronic speciation in a finite population. For quantitative characters with evolutionary parameters satisfying empirical observations and two approximate inequalities that we derived, disjunct clusters in the population flowering phenology originated within a few thousand generations in the absence of disruptive natural or sexual selection. Our simulations and the conditions we derived showed that cluster formation was promoted by limited population size, high mutational variance of flowering time, short individual flowering phenology and a long flowering season. By contrast, cluster formation was hindered by inbreeding depression, stabilizing selection and pollinator limitation. Our results suggest that incipient allochronic speciation in populations of limited size (satisfying two inequalities) could be a common phenomenon.     

Effects of assortative mating for pupa weight on genetic parameters of unselected Tribolium castaneum

Summary Effects of random (R) or positive assortative (A) mating for pupal weight (PW) on genetic parameters of pupation time (PT), pupal and larval weights (LW) were studied in unselected populations of Tribolium castaneum. Two groups, each with 50 males mated to 100 females in each of 5 replicates, were either R-mated or A-mated for 3 generations. Genetic parameters were estimated from covariances between sibs (R group) or by an iterative method (A group). Estimates of heritability in R and A groups were 0.30±0.12 and 0.39±0.02 (PW); 0.26±0.13 and 0.49±0.04 (LW); and 0.39±0.10 and 0.25±0.03 (PT). Estimates of genetic correlations in the R group were –0.21±0.23 (PW and LW); 0.45±0.10 (PW and PT); and –0.77±0.14 (LW and PT). Those in the A group were 0.27±0.10 (PW and LW); 0.15±0.14 (PW and PT); the genetic correlation between LW and PT was not estimable in this group. Within-family variances (grams squared) of PW by generation (1, 2, and 3) were, respectively: 0.048 (R) and 0.047 (A); 0.054 (R) and 0.041 (A); and 0.050 (R) and 0.046 (A). In agreement with theory, estimates of heritability of PW and LW were larger in the A group. Estimates of genetic correlations in the A group were inconsistent with expectations from theory. Assortative mating tended to decrease within-family variance of PW.     

Immunogenetic and population genetic analyses of Iberian cattle

Blood samples were collected from more than 100 animals in each of 2 Spanish cattle breeds (Retinto and De Lidia), 2 Portuguese breeds (Alentejana and Mertolenga), and American Longhorn cattle. All samples for the 4 Iberian breeds were tested for 20 polymorphic systems; American Longhorn were tested for 19 of the 20. For each breed an average inbreeding coefficient was estimated by a comparison of the observed and expected heterozygosity at 7 or 8 codominant systems tested. All breeds had positive values but only 3 breeds had estimates of inbreeding that were statistically significantly different from 0: De Lidia with = 0.17, Retinto with = 0.08 and Mertolenga with f = 0.05. The De Lidia breed especially may be suffering from inbreeding depression since this high value is greater than expected if all of the animals were progeny of half-sib matings. Genetic distances were calculated from the gene frequency data on these 5 breeds plus 9 other European breeds. Analyses of these distances show a closely related group of the 4 Iberian breeds and American Longhorn, confirming the close relationships among the Iberian breeds and the Iberian, probably Portuguese, origin of American Longhorn cattle.     

Sexual selection and assortative mating by size and their roles in the maintenance of a polymorphism in Swedish Littorina saxatilis populations

Two independent components of mating behaviour, sexual selection and assortative mating, were studied in two allopatric morphs, one sheltered boulder shore form (S-morph) and one exposed cliff shore form (E-morph), of Littorina saxatilis from the west coast of Sweden. Sexual selection was studied by comparing the sizes of copulating and non-copulating snails in the field. Size assortative mating was studied by collecting copulating pairs in the field, while assortative mating between morphs was investigated by bringing the pure morphs together in intermediary habitats and then noting the matings. The S-morph mated randomly in relation to size in two of the studied populations and exhibited a trend towards size assortative mating in a third, while the E-morph showed size assortative mating in both studied populations. The microdistribution of sizes of snails on the shores could not explain all the size assortative mating found, and instead it is argued that a size-based mate rejection behaviour also contributes to the assortative mating in at least some of these populations. There was sexual selection on size in both males and females in the S-morph, with large individuals being favoured as mates. In contrast, copulating snails of the E-morph were smaller than non-copulating ones. The significantly different sexual selection intensities between the two morphs may help to explain the size differences between them. There was random mating between the E- and the S-morphs of L. saxatilis, which suggests no incipient reproductive isolation between morphs on Swedish rocky shores. This is in agreement with earlier studies of Swedish populations, but is in contrast to the situation found in other geographical areas.     

Courtship behavior,nesting microhabitat,and assortative mating in sympatric stickleback species pairs

The maintenance of reproductive isolation in the face of gene flow is a particularly contentious topic, but differences in reproductive behavior may provide the key to explaining this phenomenon. However, we do not yet fully understand how behavior contributes to maintaining species boundaries. How important are behavioral differences during reproduction? To what extent does assortative mating maintain reproductive isolation in recently diverged populations and how important are “magic traits”? Assortative mating can arise as a by‐product of accumulated differences between divergent populations as well as an adaptive response to contact between those populations, but this is often overlooked. Here we address these questions using recently described species pairs of three‐spined stickleback (Gasterosteus aculeatus), from two separate locations and a phenotypically intermediate allopatric population on the island of North Uist, Scottish Western Isles. We identified stark differences in the preferred nesting substrate and courtship behavior of species pair males. We showed that all males selectively court females of their own ecotype and all females prefer males of the same ecotype, regardless of whether they are from species pairs or allopatric populations. We also showed that mate choice does not appear to be driven by body size differences (a potential “magic trait”). By explicitly comparing the strength of these mating preferences between species pairs and single‐ecotype locations, we were able to show that present levels of assortative mating due to direct mate choice are likely a by‐product of other adaptations between ecotypes, and not subject to obvious selection in species pairs. Our results suggest that ecological divergence in mating characteristics, particularly nesting microhabitat may be more important than direct mate choice in maintaining reproductive isolation in stickleback species pairs.     

Seasonal migration promoting assortative mating in Littorina brevicula on a boulder shore in Japan

Littorina brevicula Philippi is one of the most common snails found in the upper intertidal zone of Japan. In Amakusa, some of the population of L. brevicula migrate to the lower zone in the winter, while the rest stay in the upper zone. Thus, during the winter, which is its reproductive season, the population of L. brevicula divides into two sub-populations. This leads to a hypothesis that the migration pattern in winter is genetically controlled and this behavioural dimorphism is maintained by reproductive isolation between the two sub-populations. In order to test this hypothesis, the following three points were investigated: (1) whether the same snails migrate in a similar way every winter, (2) whether there is a significant tidal level preference in snails, and (3) whether reproductive isolation occurs between the two sub-populations. The results showed (1) the migration behaviour of each snail was consistent over two successive winters, i.e. the same group of snails migrated downward every winter and the same group of snails stayed in the upper zone every winter, (2) transplanted snails moved toward the original zones where they were caught, suggesting that the snails actively selected their tidal zone in winter, and (3) most of the snails copulated within each sub-population. Therefore, reproductive isolation between the two sub-populations was considered to be established to some extent by the dimorphic migration behaviour. In conclusion, the migratory behaviour of L. brevicula is determined separately for each individual and might be genetically controlled, and the behavioural dimorphism may be maintained by partial reproductive isolation between the two sub-populations.     

‘Prudent habitat choice’: a novel mechanism of size‐assortative mating

Assortative mating, an ubiquitous form of nonrandom mating, strongly impacts Darwinian fitness and can drive biological diversification. Despite its ecological and evolutionary importance, the behavioural processes underlying assortative mating are often unknown, and in particular, mechanisms not involving mate choice have been largely ignored so far. Here, we propose that assortative mating can arise from ‘prudent habitat choice’, a general mechanism that acts under natural selection, and that it can occur despite a complete mixing of phenotypes. We show that in the cichlid Eretmodus cyanostictus size‐assortative mating ensues, because individuals of weaker competitive ability ignore high‐quality but strongly competed habitat patches. Previous studies showed that in E. cyanostictus, size‐based mate preferences are absent. By field and laboratory experiments, here we showed that (i) habitat quality and body size are correlated in this species; (ii) territories with more stone cover are preferred by both sexes in the absence of competition; and (iii) smaller fish prudently occupy vacant territories of worse quality than do larger fish. Prudent habitat choice is likely to be a widespread mechanism of assortative mating, as both preferences for and dominance‐based access to high‐quality habitats are generic phenomena in animals.     

Genetic divergence and assortative mating between colour morphs of the sea urchin Paracentrotus gaimardi

Some species of sea urchins feature large variation in pigmentation. This variability may be the result of phenotypic plasticity or it may be associated with genetic divergence between morphs. Paracentrotus gaimardi exhibits five colour morphs (pink, brown, green, grey and black), which often occur side by side on the same rock. We studied genetic divergence between these morphs in three populations on the coast of Brazil. A fragment of the region encoding the mitochondrial ATPase 8 and 6 mitochondrial genes, a fragment of the intron of a nuclear histone and the entire nuclear gene coding for the sperm protein bindin were analysed. Mitochondrial DNA was differentiated between the pink and all other morphs, but the histone intron was similar in all colour morphs. In bindin, nine codons were found to be under positive selection and significant differences of allelic frequencies were observed in almost all pairwise comparisons between colour morphs. Although the molecular differentiation in bindin is not large enough to suggest reproductive isolation, some degree of assortative mating within morphs seems to be occurring in this species.     

Heterozygosity-based assortative mating in blue tits (Cyanistes caeruleus): implications for the evolution of mate choice

The general hypothesis of mate choice based on non-additive genetic traits suggests that individuals would gain important benefits by choosing genetically dissimilar mates (compatible mate hypothesis) and/or more heterozygous mates (heterozygous mate hypothesis). In this study, we test these hypotheses in a socially monogamous bird, the blue tit (Cyanistes caeruleus). We found no evidence for a relatedness-based mating pattern, but heterozygosity was positively correlated between social mates, suggesting that blue tits may base their mating preferences on partner''s heterozygosity. We found evidence that the observed heterozygosity-based assortative mating could be maintained by both direct and indirect benefits. Heterozygosity reflected individual quality in both sexes: egg production and quality increased with female heterozygosity while more heterozygous males showed higher feeding rates during the brood-rearing period. Further, estimated offspring heterozygosity correlated with both paternal and maternal heterozygosity, suggesting that mating with heterozygous individuals can increase offspring genetic quality. Finally, plumage crown coloration was associated with male heterozygosity, and this could explain unanimous mate preferences for highly heterozygous and more ornamented individuals. Overall, this study suggests that non-additive genetic traits may play an important role in the evolution of mating preferences and offers empirical support to the resolution of the lek paradox from the perspective of the heterozygous mate hypothesis.     

The strength of assortative mating for flowering date and its basis in individual variation in flowering schedule

Although it has been widely asserted that plants mate assortatively by flowering time, there is virtually no published information on the strength or causes of phenological assortment in natural populations. When strong, assortative mating can accelerate the evolution of plant reproductive phenology through its inflationary effect on genetic variance. We estimated potential assortative mating for flowering date in 31 old‐field species in Ontario, Canada. For each species, we constructed a matrix of pairwise mating probabilities from the individual flowering schedules, that is the number of flower deployed on successive dates. The matrix was used to estimate the phenotypic correlation between mates, ρ, for flowering date. We also developed a measure of flowering synchrony within species, S, based upon the eigenstructure of the mating matrix. The mean correlation between pollen recipients and potential donors for flowering date was  = 0.31 (range: 0.05–0.63). A strong potential for assortative mating was found among species with high variance in flowering date, flowering schedules of short duration and skew towards early flower deployment. Flowering synchrony, S, was negatively correlated with potential assortment (r = ?0.49), but we go on to show that although low synchrony is a necessary condition for phenological assortative mating, it may not be sufficient to induce assortment for a given phenological trait. The potential correlation between mates showed no seasonal trend; thus, as climate change imposes selection on phenology through longer growing seasons, spring‐flowering species are no more likely to experience an accelerated evolutionary response than summer species.     

Clinal variation in morphology and assortative mating in the soldier beetle, Chauliognathus pennsylvanicus (Goleoptera: Cantharidae)

In north Georgia populations of the soldier beetle, Chauliognathus pennsylvanicus , the length of the elytral spot varies clinally. At the southern end of a 200 km cline the distribution of spot length is unimodal with longer spot lengths predominating while at the northern end of the cline the distribution is bimodal but with shorter spot lengths being more frequent. North of the cline only short elytral spot lengths are observed, while the converse is true south of the cline. The strength of assortative mating on the basis of elytral spot length increases from south to north along the cline, resulting in complete pre-mating isolation between short and long spot length morphs at the north end of the cline. Laboratory mate choice tests indicate that assortative mating in the field is not the result of differential timing of activity or microhabitat choice but rather that it represents a real behavioural preference. Individuals from monomorphic populations on either side of the cline do not mate assortatively in the laboratory, indicating that reproductive isolation has evolved on the cline.