How Individualized Niches Arise: Defining Mechanisms of Niche Construction, Niche Choice, and Niche Conformance.

Organisms interact with their environments in various ways. We present a conceptual framework that distinguishes three mechanisms of organism-environment interaction. We call these NC3 mechanisms: niche construction, in which individuals make changes to the environment; niche choice, in which individuals select an environment; and niche conformance, in which individuals adjust their phenotypes in response to the environment. Each of these individual-level mechanisms affects an individual's phenotype-environment match, its fitness, and its individualized niche, defined in terms of the environmental conditions under which the individual can survive and reproduce. Our framework identifies how individuals alter the selective regimes that they and other organisms experience. It also places clear emphasis on individual differences and construes niche construction and other processes as evolved mechanisms. The NC3 mechanism framework therefore helps to integrate population-level and individual-level research.

Male social niche conformance? Effects of manipulated opportunity for extra-pair mating on behavior and hormones of male zebra finches.

Success in sperm competition is an important determinant of male fitness in mating systems with female multiple mating. Thus, sperm competition risk represents a key dimension of the male social environment to which individual males are expected to adaptively adjust their reproductive phenotype. Such adaptive phenotypic adjustment we here refer to as male social niche conformance. In this pre-registered study, we investigated how male zebra finches, Taeniopygia guttata, adjust their behavior to sperm competition risk. We experimentally manipulated the opportunity for extra-pair mating to create two levels of sperm competition risk: 1) Single-pair, no sperm competition risk; 2) Double-pair, sperm competition risk. We compared male courtship, mate guarding, copulation rates, and aggression between the treatment groups. To identify hormonal correlates of male behavioral adjustment, we measured plasma testosterone and corticosterone levels before and after the social treatment started. Contrary to our pre-registered predictions, males from the Double-pair treatment group decreased courtship rates compared to those from the Single-pair group, and Double-pair males responded less aggressively towards intruders than Single-pair males. Testosterone levels decreased over the breeding cycle, but social treatment had no effect on either testosterone or corticosterone levels. Our results indicate that male zebra finches do not intensify courtship or competitive reproductive behaviors, or upregulate key hormones when another breeding pair is present. Although we found no evidence for the predicted adaptive behavioral responses to sperm competition risk, we show that male zebra finches plastically adjust their behavior to their social environment.

Sperm velocity in a promiscuous bird across experimental media of different viscosities.

In species with internal fertilization, the female genital tract appears challenging to sperm, possibly resulting from selection on for example ovarian fluid to control sperm behaviour and, ultimately, fertilization. Few studies, however, have examined the effects of swimming media viscosities on sperm performance. We quantified effects of media viscosities on sperm velocity in promiscuous willow warblers Phylloscopus trochilus. We used both a reaction norm and a character-state approach to model phenotypic plasticity of sperm behaviour across three experimental media of different viscosities. Compared with a standard medium (Dulbecco's Modified Eagle Medium, DMEM), media enriched with 1% or 2% w/v methyl cellulose decreased sperm velocity by up to about 50%. Spermatozoa from experimental ejaculates of different males responded similarly to different viscosities, and a lack of covariance between elevations and slopes of individual velocity-by-viscosity reaction norms indicated that spermatozoa from high- and low-velocity ejaculates were slowed down by a similar degree when confronted with high-viscosity environments. Positive cross-environment (1% versus 2% cellulose) covariances of sperm velocity under the character-state approach suggested that sperm performance represents a transitive trait, with rank order of individual ejaculates maintained when expressed against different environmental backgrounds. Importantly, however, a lack of significant covariances in sperm velocity involving a cellulose concentration of 0% indicated that pure DMEM represented a qualitatively different environment, questioning the validity of this widely used standard medium for assaying sperm performance. Enriching sperm environments along ecologically relevant gradients prior to assessing sperm performance will strengthen explanatory power of in vitro studies of sperm behaviour.

Moderate heritability and low evolvability of sperm morphology in a species with high risk of sperm competition, the collared flycatcher Ficedula albicollis.

Spermatozoa represent the morphologically most diverse type of animal cells and show remarkable variation in size across and also within species. To understand the evolution of this diversity, it is important to reveal to what degree this variation is genetic or environmental in origin and whether this depends on species' life histories. Here we applied quantitative genetic methods to a pedigreed multigenerational data set of the collared flycatcher Ficedula albicollis, a passerine bird with high levels of extra-pair paternity, to partition genetic and environmental sources of phenotypic variation in sperm dimensions for the first time in a natural population. Narrow-sense heritability (h2 ) of total sperm length amounted to 0.44 ± 0.14 SE, whereas the corresponding figure for evolvability (estimated as coefficient of additive genetic variation, CVa ) was 0.02 ± 0.003 SE. We also found an increase in total sperm length within individual males between the arrival and nestling period. This seasonal variation may reflect constraints in the production of fully elongated spermatozoa shortly after arrival at the breeding grounds. There was no evidence of an effect of male age on sperm dimensions. In many previous studies on laboratory populations of several insect, mammal and avian species, heritabilities of sperm morphology were higher, whereas evolvabilities were similar. Explanations for the differences in heritability may include variation in the environment (laboratory vs. wild), intensity of sexual selection via sperm competition (high vs. low) and genetic architecture that involves unusual linkage disequilibrium coupled with overdominance in one of the studied species.

Social competition as a driver of phenotype-environment correlations: implications for ecology and evolution.

While it is universally recognised that environmental factors can cause phenotypic trait variation via phenotypic plasticity, the extent to which causal processes operate in the reverse direction has received less consideration. In fact individuals are often active agents in determining the environments, and hence the selective regimes, they experience. There are several important mechanisms by which this can occur, including habitat selection and niche construction, that are expected to result in phenotype-environment correlations (i.e. non-random assortment of phenotypes across heterogeneous environments). Here we highlight an additional mechanism - intraspecific competition for preferred environments - that may be widespread, and has implications for phenotypic evolution that are currently underappreciated. Under this mechanism, variation among individuals in traits determining their competitive ability leads to phenotype-environment correlation; more competitive phenotypes are able to acquire better patches. Based on a concise review of the empirical evidence we argue that competition-induced phenotype-environment correlations are likely to be common in natural populations before highlighting the major implications of this for studies of natural selection and microevolution. We focus particularly on two central issues. First, competition-induced phenotype-environment correlation leads to the expectation that positive feedback loops will amplify phenotypic and fitness variation among competing individuals. As a result of being able to acquire a better environment, winners gain more resources and even better phenotypes - at the expense of losers. The distinction between individual quality and environmental quality that is commonly made by researchers in evolutionary ecology thus becomes untenable. Second, if differences among individuals in competitive ability are underpinned by heritable traits, competition results in both genotype-environment correlations and an expectation of indirect genetic effects (IGEs) on resource-dependent life-history traits. Theory tells us that these IGEs will act as (partial) constraints, reducing the amount of genetic variance available to facilitate evolutionary adaptation. Failure to recognise this will lead to systematic overestimation of the adaptive potential of populations. To understand the importance of these issues for ecological and evolutionary processes in natural populations we therefore need to identify and quantify competition-induced phenotype-environment correlations in our study systems. We conclude that both fundamental and applied research will benefit from an improved understanding of when and how social competition causes non-random distribution of phenotypes, and genotypes, across heterogeneous environments.

Genotype-by-environment interactions for precopulatory mate guarding in a lek-mating insect.

In sexually reproducing species, males often experience strong pre- and postcopulatory sexual selection leading to a wide variety of male adaptations. One example is mate guarding, where males prevent females from mating with other males either before or after they (will) have mated themselves. In case social conditions vary short term and in an unpredictable manner and if there is genetic variation in plasticity of mate guarding (i.e., genotype-by-environment interaction, G × E), adaptive behavioral plasticity in mate guarding may evolve. Here, we test for genetic variation in the plasticity of precopulatory mate-guarding behavior in the lek-mating lesser wax moth Achroia grisella. When offered two females in rapid succession, virgin males of this species usually copulate around 10-20 min with the first female. With the second female, however, they engage in copulation posture for many hours until they have produced another spermatophore, an unusual behavior among insects possibly functioning as precopulatory mate guarding. Previous studies showed the mating latency with the second female to be shorter under higher perceived sperm competition risk. We accordingly measured the mate-guarding behavior of males from six inbred lines under either elevated perceived male-male competition risk or under control conditions allowing us to test for G × E interactions. We found significant inbred line-by-competitor treatment interactions on mating latency and copulation duration with the second female suggesting genetic variation in the degree of behavioral plasticity. However, we found no significant G × E interaction on the sum of mating latency and copulation duration. Our results suggest a potential for adaptive evolution of mate-guarding plasticity in natural populations of lek-mating species. Future studies using selection experiments and experimental evolution approaches in laboratory populations, or comparisons of multiple natural populations will be helpful to study under which conditions plasticity in male mate-guarding behavior evolves.

Lifespan, lifetime reproductive performance and paternity loss of within-pair and extra-pair offspring in the coal tit Periparus ater.

The hypothesis that females of socially monogamous species obtain indirect benefits (good or compatible genes) from extra-pair mating behaviour has received enormous attention but much less generally accepted support. Here we ask whether selection for adult survival and fecundity or sexual selection contribute to indirect selection of the extra-pair mating behaviour in socially monogamous coal tits (Periparus ater). We tracked locally recruited individuals with known paternity status through their lives predicting that the extra-pair offspring (EPO) would outperform the within-pair offspring (WPO). No differences between the WPO and EPO recruits were detected in lifespan or age of first reproduction. However, the male WPO had a higher lifetime number of broods and higher lifetime number of social offspring compared with male EPO recruits, while no such differences were evident for female recruits. Male EPO recruits did not compensate for their lower social reproductive success by higher fertilization success within their social pair bonds. Thus, our results do not support the idea that enhanced adult survival, fecundity or within-pair fertilization success are manifestations of the genetic benefits of extra-pair matings. But we emphasize that a crucial fitness component, the extra-pair fertilization success of male recruits, has yet

Yearling male great tits, Parus major, suffer more strongly from cuckoldry than older males.

In the majority of socially monogamous bird species, females have offspring sired by males other than their social mate as the result of extra-pair copulations. While it is widely recognised that there is considerable variation in the frequency of extra-pair paternity between species, between populations of a species and between individuals of a population, determinants of this variation are surprisingly difficult to establish. With respect to individual variation within a population, it is an important step to test for male and female correlates of cuckoldry to better understand the patterns as well as the adaptive significance of extra-pair mating behaviour. Here, we analysed patterns of extra-pair paternity in relation to male age, female age and their interaction in the great tit Parus major, a socially monogamous passerine with a moderate frequency of extra-pair paternity. Based on a large sample of 316 genotyped first broods from five successive years, we failed to demonstrate interaction effects of male and female age on both the proportion of extra-pair offspring and the likelihood that at least one extra-pair offspring is present within a brood. However, both the proportion of extra-pair offspring and the likelihood of paternity loss were higher for yearling as compared to older males, while this was not the case for yearling vs. older females. Furthermore, the proportion of extra-pair offspring within a brood decreased with increasing age of the attending male in within-individual analyses. We found a comparable effect also for attending females in within-individual analyses, but only when excluding two individuals with 100% extra-pair paternity. A female (extra-pair) mating preference for older males and/or a limited ability of yearling males to prevent cuckoldry in their broods could explain these age-related patterns of paternity loss. Effect sizes, however, were not particularly large and substantial residual variation within age categories suggests the importance of further yet unidentified determinants of variation in paternity loss in the study population.

Sex-specific repeatabilities and effects of relatedness and mating status on copulation duration in an acridid grasshopper.

In species with direct sperm transfer, copulation duration is a crucial trait that may affect male and female reproductive success and that may vary with the quality of the mating partner. Furthermore, traits such as copulation duration represent the outcome of behavioral interactions between the sexes, for which it is important-but often difficult-to determine which sex is in phenotypic control. Using a double-mating protocol, we compared copulation durations between (1) virgin and nonvirgin and (2) sibling and nonsibling mating pairs in rufous grasshoppers Gomphocerippus rufus. Nonvirgin copulations took on average approximately 30% longer than virgin copulations, whereas relatedness of mating partners was not a significant predictor of copulation duration. Longer nonvirgin copulations may represent a male adaptation to sperm competition if longer copulations allow more sperm to be transferred or function as postinsemination mate guarding. The absence of differences between pairs with different degrees of relatedness suggests no precopulatory or preinsemination inbreeding avoidance mechanism has evolved in this species, perhaps because there is no inbreeding depression in this species, or because inbreeding avoidance occurs after copulation. Controlling for the effects of male and female mating status (virgin vs. nonvirgin) and relatedness (sibling vs. nonsibling), we found significant repeatabilities (R) in copulation duration for males (R = 0.33; 95% CI: 0.09-0.55) but not for females (R = 0.09; 95% CI: 0.00-0.30). Thus, copulation durations of males more strongly represent a nontransient trait expressed in a consistent manner with different mating partners, suggesting that some aspect of the male phenotype may determine copulation duration in this species. However, overlapping confidence intervals for our sex-specific repeatability estimates indicate that higher sampling effort is required for conclusive evidence.

Paternal genetic effects on offspring fitness are context dependent within the extrapair mating system of a socially monogamous passerine.

Avian extrapair mating systems provide an interesting model to assess the role of genetic benefits in the evolution of female multiple mating behavior, as potentially confounding nongenetic benefits of extrapair mate choice are seen to be of minor importance. Genetic benefit models of extrapair mating behavior predict that females engage in extrapair copulations with males of higher genetic quality compared to their social mates, thereby improving offspring reproductive value. The most straightforward test of such good genes models of extrapair mating implies pairwise comparisons of maternal half-siblings raised in the same environment, which permits direct assessment of paternal genetic effects on offspring traits. But genetic benefits of mate choice may be difficult to detect. Furthermore, the extent of genetic benefits (in terms of increased offspring viability or fecundity) may depend on the environmental context such that the proposed differences between extrapair offspring (EPO) and within-pair offspring (WPO) only appear under comparatively poor environmental conditions. We tested the hypothesis that genetic benefits of female extrapair mate choice are context dependent by analyzing offspring fitness-related traits in the coal tit (Parus ater) in relation to seasonal variation in environmental conditions. Paternal genetic effects on offspring fitness were context dependent, as shown by a significant interaction effect of differential paternal genetic contribution and offspring hatching date. EPO showed a higher local recruitment probability than their maternal half-siblings if born comparatively late in the season (i.e., when overall performance had significantly declined), while WPO performed better early in the season. The same general pattern of context dependence was evident when using the number of grandchildren born to a cuckolding female via her female WPO or EPO progeny as the respective fitness measure. However, we were unable to demonstrate that cuckolding females obtained a general genetic fitness benefit from extrapair fertilizations in terms of offspring viability or fecundity. Thus, another type of benefit could be responsible for maintaining female extrapair mating preferences in the study population. Our results suggest that more than a single selective pressure may have shaped the evolution of female extrapair mating behavior in socially monogamous passerines.

Determinants of between-year burrow re-occupation in a colony of the European bee-eater Merops apiaster.

Re-occupation of existing nesting burrows in the European bee-eater Merops apiaster has only rarely - and if so mostly anecdotically - been documented in the literature record, although such behavior would substantially save time and energy. In this study, we quantify burrow re-occupation in a German colony over a period of eleven years and identify ecological variables determining reuse probability. Of 179 recorded broods, 54% took place in a reused burrow and the overall probability that one of 75 individually recognized burrows would be reused in a given subsequent year was estimated as 26.4%. This indicates that between-year burrow reuse is a common behavior in the study colony which contrasts with findings from studies in other colonies. Furthermore, burrow re-occupation probability declined highly significantly with increasing age of the breeding wall. Statistical separation of within- and between-burrow effects of the age of the breeding wall revealed that a decline in re-occupation probability with individual burrow age was responsible for this and not a selective disappearance of burrows with high re-occupation probability over time. Limited duty cycles of individual burrows may be caused by accumulating detritus or decreasing stability with increasing burrow age. Alternatively, burrow fidelity may presuppose pair fidelity which may also explain the observed restricted burrow reuse duty cycles. A consequent next step would be to extend our within-colony approach to other colonies and compare the ecological circumstances under which bee-eaters reuse breeding burrows.

Long-term fitness consequences of female extra-pair matings in a socially monogamous passerine.

Whether female birds choose extra-pair mating partners to obtain genetic fitness benefits is intensely debated. The most straightforward and crucial test of 'good genes' models of female extra-pair mating is the comparison of naturally 'cross-fostered' maternal half-siblings sharing the same rearing environment as any systematic differences in performance between the two categories of offspring phenotype can be attributed to differential paternal genetic contribution. We analysed local recruitment and first-year reproductive performance of maternal half-siblings in the coal tit (Parus ater), a passerine bird with high levels of extra-pair paternity. We provide a highly comprehensive measure of the long-term fitness consequences of female extra-pair matings based on a large sample of 736 within-pair offspring (WPO) and 368 extra-pair offspring (EPO) from 91 first and 55 second broods, from which 132 breeders recruited into the study population. In contrast to predictions derived from 'good genes' models, we found no differences in local recruitment and seven parameters of first-year reproductive performance when comparing WPO and EPO. These results question the universal validity of findings in other bird species supporting 'good genes' models, particularly as they are based on the best approximation to female fitness obtained so far.

Differential sperm expenditure reveals a possible role for post-copulatory sexual selection in a lekking moth.

Male reproductive success in the lesser wax moth Achroia grisella is strongly determined by pre-copulatory mate choice, during which females choose among males aggregated in small leks based on the attractiveness of ultrasonic songs. Nothing is known about the potential of post-copulatory mechanisms to affect male reproductive success. However, there is evidence that females at least occasionally remate with a second male and that males are unable to produce ejaculates quickly after a previous copulation. Here we investigated the effects of mating history on ejaculate size and demonstrate that the number of transferred sperm significantly decreased from first (i.e., virgin) to second (i.e., nonvirgin) copulation within individual males. For males of identical age, the number of sperm transferred was higher in virgin than in nonvirgin copulations, too, demonstrating that mating history, is responsible for the decrease in sperm numbers transferred and not the concomitant age difference. Furthermore, the number of transferred sperm was significantly repeatable within males. The demonstrated variation in ejaculate size both between subsequent copulations as well as among individuals suggests that there is allocation of a possibly limited amount of sperm. Because female fecundity is not limited by sperm availability in this system, post-copulatory mechanisms, in particular sperm competition, may play a previously underappreciated role in the lesser wax moth mating system.

Comment on "Bateman in nature: predation on offspring reduces the potential for sexual selection".

Byers and Dunn's (Reports, 9 November 2012, p.802) conclusion that predation constrains sexual selection is problematic for three reasons: their nonstandard calculation of Bateman slopes; their assertion that random processes do not influence reproductive success; and the statistically unjustifiable use of 6 variables to explain just 10 observations.

No evidence for pre-copulatory sexual selection on sperm length in a passerine bird.

There is growing evidence that post-copulatory sexual selection, mediated by sperm competition, influences the evolution of sperm phenotypes. Evidence for pre-copulatory sexual selection effects on sperm traits, on the other hand, is rather scarce. A recent paper on the pied flycatcher, Ficedula hypoleuca, reported phenotypic associations between sperm length and two sexually selected male traits, i.e. plumage colour and arrival date, thus invoking pre-copulatory sexual selection for longer sperm. We were unable to replicate these associations with a larger data set from the same and two additional study populations; sperm length was not significantly related to either male plumage colour or arrival date. Furthermore, there was no significant difference in sperm length between populations despite marked differences in male plumage colour. We also found some evidence against the previously held assumption of longer sperm being qualitatively superior; longer sperm swam at the same speed as shorter sperm, but were less able to maintain speed over time. We argue that both empirical evidence and theoretical considerations suggest that the evolution of sperm morphology is not primarily associated with pre-copulatory sexual selection on male secondary sexual traits in this or other passerine bird species. The relatively large between-male variation in sperm length in this species is probably due to relaxed post-copulatory sexual selection.

Extra-pair sires as identified by means of standardized across-gel comparisons of multilocus DNA fingerprints.

Molecular analyses of genetic parentage in wild bird populations demonstrate that extra-pair paternity (EPP) is common, even in socially monogamous species. After having identified extra-pair offspring (EPO), an important step is to uncover the identity of extra-pair sires (EPS). Studies relying on multilocus DNA fingerprinting face the problem that simple between-gel comparisons of fingerprint banding patterns are imprecise in assigning parentage across gels. To tackle this problem, we developed a method to identify EPS by means of standardized across-gel comparisons of multilocus DNA fingerprints and applied it in a socially monogamous bird species with high levels of EPP, the coal tit (Parus ater). Scanned DNA fingerprint gels and standard image-editing software allowed to screen and reliably identify EPS. Overall, EPP was successfully assigned to 32 different EPS for 143 out of 210 (68.1%) EPO detected. This corresponds well to extra-pair parentage assignment rates revealed by microsatellite-based studies in congeneric species. Our approach proves especially useful whenever multilocus DNA fingerprints for parentage exclusion exist while microsatellite markers are not available.