Biology subjects

Kempenaers, B.

Publications and source records attributed to Kempenaers, B..

At least 19 recordsLinked to original sources

bioRxiv2025

The germline-restricted chromosome orchestrates germ cell development in passerine birds

While the definition of germ cell fate has been extensively studied in model organisms, evolutionary innovations and mechanistic novelties may remain hidden in understudied systems. The phenomenon of programmed DNA elimination allows germ cells to acquire germline-restricted genes, offering a novel paradigm of germ cell specificity. In passerine birds, the germline-restricted chromosome (GRC) is eliminated from somatic cells in early embryogenesis, yet the role and consequences of its maintenance in the germ cells remain poorly understood. Here, using the zebra finch Taeniopygia guttata as a model, we combined RNA-seq and Spatial Transcriptomics to construct a high-resolution spatiotemporal expression map to understand the role of the GRC across germ cell development. We found a GRC-linked integrin-BMP signaling in maturing oocytes and tfebGRC upregulation at blastoderm embryos, suggesting the involvement of the GRC in oocyte maturation and germ cell determination. We also identified developmental specialization of GRC-linked gene expression relative to their paralogs on the autosomes and sex chromosomes, revealing a gene repertoire which promotes germline stemness and germline/soma distinction. Together, the passerine GRC constitutes a unique system that manifests germ cell complexity, whilst allowing pinpointing the effects on gene expression that may elucidate vertebrate germ cell fate.

developmental biology↗

bioRxiv2025

Sex differences in development alter the fledgling sex ratio in a lekking bird with strong sexual size dimorphism

Sex ratio variation is of fundamental importance for population ecology, and the evolution of sex roles and life-histories. Yet, the ecological mechanisms underlying such variation remain often unknown. Using a multiyear dataset from captive and wild precocial Ruffs Calidris pugnax, we show that poorer survival and later fledging of males relative to females result in a female biased sex ratio of the fledgling population. Both sex-specific survival and maturation time contributed equally to an increasing sex ratio bias from hatching to fledging in this sexually dimorphic bird. On average, juvenile females fledged three days earlier than males due to expedited wing development, despite the higher absolute rate of wing growth in males. We argue that sex differences in growth, maturation, and offspring survival are likely the result of strong pre-sexual selection on males to achieve dominance and may help to enforce the Darwinian sex roles observed in this species.

ecology↗

bioRxiv2025

Programmed DNA elimination drives rapid genomic innovation in two thirds of all bird species

Bird genomes are among the most stable in terms of synteny and gene content across vertebrates. However, germline-restricted chromosomes (GRCs) represent a striking exception where programmed DNA elimination confines large-scale genomic changes to the germline. GRCs are known to occur in songbirds (oscines), but have been studied only in a few species of Passerides such as the zebra finch, the key model for passerine genomics. Their presence and evolutionary dynamics in most major passerine lineages remain largely unexplored, with suboscines entirely unexamined by cytogenetic or genomic methods. Here, we present the most comprehensive comparative analysis of GRCs to date, spanning 44 million years of passerine evolution. By generating the first germline reference genomes of an oscine and a suboscine, 22 novel germline draft genomes spanning nearly all major passerine lineages and a germline draft genome of a parrot outgroup, we show that the GRC is likely present in 6,700 passerine species. Our results reveal that the GRC evolves rapidly and distinctly from the standard A chromosomes (autosomes and sex chromosomes), yet retains functionally important, selectively maintained genes. We observed gene and repeat turnover occuring orders of magnitude faster than on the A chromosomes. Some GRC genes, such as cpeb1 and pim1, are widespread from an ancient duplication. In contrast, other GRC genes, like mfsd2b and bmp15, have been independently duplicated onto the GRC multiple times, suggesting adaptive constraints. The discovery of zglp1 on the zebra finch GRC, initially copied from chromosome 30 and subsequently lost from it, indicates functional replacement, where the GRC permits gene loss from the standard genome. As the GRC harbors the only zglp1 copy in most of the [~]4000 Passerides species, GRC loss would compromise essential germline functions. Our findings establish the GRC as a genomic innovator driving rapid germline evolution. This fact highlights its evolutionary significance for passerine diversification and suggests that programmed DNA elimination may be an overlooked yet phylogenetically widespread mechanism in many understudied animal lineages.

genomics↗

bioRxiv2025

Conspecific brood parasitism in the barn swallow (Hirundo rustica)

Conspecific brood parasitism (CBP) has been reported in many altricial avian species, yet its prevalence and underlying behavioural mechanisms remain poorly understood. We studied CBP in the barn swallow (Hirundo rustica), a species in which conspecific brood parasitism has been reported. We conducted parentage analysis on 1945 barn swallow broods involving 7816 offspring. Samples were collected over 12 breeding seasons at 5 colonies/populations. Contrary to expectations, we identified only six cases of CBP (0.3 % of broods). By identifying all individuals involved, i.e. the parasitic females, the female hosts and the males that fathered the parasitic eggs, we determined these cases of CBP resulted most likely from either a failed nest take-over (three times), the disappearance of a female partner or a disruption caused by researchers while only one case could be interpreted as a result of females mixed reproductive tactic. Based on a review of the literature on CBP in seven other Hirundinidae, we conclude that the only reliable evidence for CBP comes from cliff swallows (Petrochelidon pyrrhonata). Studies on other species either failed to identify the parasitic females or do not present sufficient evidence supporting the occurrence of CBP. Several studies relied on the appearance of two eggs in a nest within 24 hours to conclude that CBP occurred. However, based on the parentage analysis, we show that CBP only occurred in one out of 11 such cases in our barn swallow data. Our findings highlight that CBP is rare in our barn swallow populations, and have been likely overestimated in other studies. We emphasize the importance of frequent nest checks and rigorous genetic validation in CBP research. Overall, our results challenge existing assumptions about the prevalence of CBP and provide insights into the behavioural mechanisms that lead to CBP, with ecological and evolutionary implications.

ecology↗

bioRxiv2024

Sex and morph variation in activity from early ontogeny to maturity in ruffs (Calidris pugnax)

Intraspecific variation provides the substrate for the evolution of organisms. Ruffs show exceptional phenotypic variation in physiology, appearance and behaviour linked to variation between sexes and male alternative reproductive tactics (ARTs). The male ARTs are associated with the evolution of separate morphs, which are encoded by an autosomal supergene. However, the effects of the supergene on females and chicks are much less well understood. In particular, it is still unknown, whether females also show morph-specific behavioural variation, when behavioural differences emerge during ontogeny, and whether behavioural differences can be detected outside of the breeding context. To address these knowledge gaps, we repeatedly measured the activity in an unfamiliar environment, also known as exploration behaviour, of 109 hand-raised young ruffs throughout their first two years of life. We used automated tracking in an open field arena, and quantified the distance moved within 10 minutes to examine behavioural differences between sexes, morphs and individuals. The activity of young ruffs rapidly increased during the first month after their crouching reflex, a response to potential threats, subsided. Repeatability of individual activity was initially low but increased throughout juvenile ontogeny and was high (R = 0.5) from day 21 onwards. Variation in activity was clearly sex-linked with females moving more than males, indicating potential energetic trade-offs accompanying the strong sexual size dimorphism. In contrast, morph differences in activity remained inconsistent and elusive, both in females and in males. Our results indicate that in species where much of the known behavioural variation is linked to mating tactics, a non-reproductive behaviour can show between-individual variation and clear sex differences, whereas morph differences appear less pronounced.

animal behavior and cognition↗

bioRxiv2024

The collective application of shorebird tracking data to conservation

Addressing urgent conservation issues, like the drastic declines of North American migratory birds, requires creative, evidence-based, efficient, and collaborative approaches. Over 50% of monitored North American shorebird populations have lost over 50% of their abundance since 1980. To address these declines, we developed a partnership of scientists and practitioners called the Shorebird Science and Conservation Collective (hereinafter "the Collective"). Here, we present this successful case study as an example for others engaged in translational science. The Collective acts as an intermediary whereby dedicated staff collate and analyze data contributions from scientists to support knowledge requests from conservation practitioners. Data contributions from 74 organizations include over 6.7 million shorebird locations forming movement paths of 3,345 individuals representing 36 species tracked across the Americas. We describe the founding and structure of the Collective and conservation activities we supported in our first two years. As the volume of scientific data on animal movements continues to grow, groups like the Collective can be vital liaisons to rapidly integrate and interpret research to support conservation action.

ecology↗

bioRxiv2023

Sperm traits of the three genetic morphs in the ruff sandpiper

BackgroundThe ruff sandpiper Calidris pugnax is a Palearctic lekking shorebird with three genetic morphs determined by an autosomal inversion. Male morphs differ strikingly in body size, ornaments, endocrinology and mating behavior. Aggressive Independents represent the ancestral haplotype, while female-mimicking Faeders and semi-cooperative Satellites are the inverted haplotypes. Because one inversion breakpoint is homozygous lethal, the inverted haplotypes cannot recombine and are expected to accumulate deleterious mutations. The inversion regions also harbor genes involved in spermatogenesis. However, it remains unknown whether the genetic differences between the morphs also translate into differences in sperm traits. Here, we use a captive-bred population of ruffs to compare sperm swimming speed and morphology among the morphs. ResultsRuff sperm morphologically resembled those of passerines, but moved differently, vibrating from side to side while slowly moving forward, rather than rotating while moving forward. Faeder sperm moved the slowest, which is consistent with the prediction of genetic deterioration over time. However, against expectation, sperm of Independents did not seem to be of the highest quality, i.e., their sperm were not the fastest nor the least variable, and they had sperm with the shortest tail and midpiece. Although the midpiece contains the energy-producing mitochondria, sperm midpiece length was not associated with sperm swimming speed. Instead, two of three velocity metrics weakly positively correlated with head length (absolute and relative). ConclusionsThe three genetically determined ruff morphs showed subtle differences in swimming speed and in the length of some sperm components. However, the between-morph differences in sperm swimming speed were not linked to the differences in morphology. We conclude that there is at best limited evidence for lower-quality sperm in the morphs that carry the inversion, and suggest that the potential for the evolution of morph-specific sperm adaptations may be limited in this system. Lay SummaryThe ruff sandpiper is a shorebird that exhibits three genetically distinct types of males, which differ markedly in body size, ornaments, hormones, and mating behavior. Aggressive Independents represent the type that evolved first. Semi-cooperative Satellites and female-mimicking Faeders evolved later through a specific type of genetic rearrangement called an inversion, in which a segment of a chromosome reversed in orientation. Due to the nature of this inversion, Satellite and Faeder chromosomes are expected to deteriorate over time. However, it remains unclear whether the genetic differences between these morphs, which affect physiological and behavioral traits, also translate into differences in sperm traits. We used a captive population of ruffs to compare sperm swimming speed and length measurements between the three types of males. Faeder sperm was the slowest, which is consistent with expectations based on genetic deterioration over time. However, against our expectations, the sperm of Independents does not appear to have better performance characteristics. Although the midpiece of a sperm is responsible for energy production, the length of the midpiece did not relate to sperm swimming speed.

evolutionary biology↗

bioRxiv2021

Nest relief in the cryptically-incubating semipalmated sandpiper is quick but vocal

Biparental care requires coordination between parents. Such coordination might prove difficult if opportunities to communicate are scarce, which might have led to the evolution of elaborate and noisy nest relief rituals in species facing a low risk of predation. However, whether such conspicuous rituals also evolved in species that avoid predation by relying on crypsis remains unclear. Here, we used a continuous monitoring system to describe nest relief behavior during incubation in an Arctic-breeding shorebird with passive nest defense, the semipalmated sandpiper (Calidris pusilla). We then explored whether nest relief behavior provides information about parental cooperation and predicts incubation effort. We found that incubating parents vocalized twice as much before the arrival of their partner than during other times of incubation. In 75% of nest reliefs, the incubating parent left the nest only after its partner had returned and initiated the nest relief. In these cases, exchanges were quick (25s, median) and shortened over the incubation period by 0.1 - 1.4s per day (95%CI), suggesting that parents became more synchronized. However, nest reliefs were not cryptic. In 90% of exchanges, at least one parent vocalized, and in 20% of nest reliefs the incubating parent left the nest only after its returning partner called instantaneously. In 30% of cases, the returning parent initiated the nest relief with a call; in 39% of these cases, the incubating partner replied. If the partner replied, the next off-nest bout was 1 - 4hr (95%CI) longer than when the partner did not reply, which corresponds to an 8 - 45% increase. Our results indicate that incubating semipalmated sandpipers, which rely on crypsis to avoid nest predation, have quick but acoustically conspicuous nest reliefs. Our results also suggest that vocalizations during nest reliefs may be important for the division of parental duties. LAY SUMMARYO_LIBiparental care requires coordination between parents. In species where both parents incubate and nests are visible, parents often perform complex nest relief rituals. Is this also the case in species where nests are cryptic? C_LIO_LIWe video-recorded nest relief behavior at nests of cryptically incubating semipalmated sandpipers. C_LIO_LIParents relieved each other quickly, but they vocalized frequently. In 20% of nest reliefs the incubating parent left only after its returning partner called instantaneously. In 30% of cases the returning parent initiated the nest relief with a call. If the partner replied, its next off-nest bout was 1 - 4hr longer than when the partner did not reply, which corresponds to an 8 - 45% increase. C_LIO_LIOur results suggest that vocalizations during nest relief may be important for the division of parental duties. Further work in sandpipers and other taxa is needed to elucidate the role of parental vocalization in coordinating and synchronizing parental duties. C_LI

animal behavior and cognition↗

bioRxiv2021

Fitness costs of female choosiness in a socially monogamous songbird

Female mate choice is thought to be responsible for the evolution of many extravagant male ornaments and displays, but the costs of being too selective may hinder the evolution of choosiness. Selection against choosiness should be strongest in socially monogamous mating systems, because females may end up without a partner and forego reproduction, especially when many females prefer the same few partners (frequency-dependent selection). Here we quantify the fitness costs of having mating preferences that are difficult to satisfy. We capitalise on the recent discovery that female zebra finches (Taeniopygia guttata) prefer males of familiar song dialect. We measured female fitness in captive breeding colonies in which one third of females were given ample opportunity to choose a mate of their preferred dialect (two thirds of all males; relaxed competition), while two thirds of the females had to compete over a limited pool of mates they preferred (one third of all males; high competition). As expected, social pairings were strongly assortative with regard to song dialect. In the high-competition group, 26% of the females remained unpaired, yet they still obtained relatively high fitness by using brood parasitism as an alternative reproductive tactic. Another 31% of high-competition females paired disassortatively for song dialect. These females showed increased levels of extra-pair paternity, mostly with same-dialect males as sires, suggesting that preferences were not abolished after social pairing. However, females that paired disassortatively for song dialect did not have lower reproductive success. Overall, females in the high-competition group reached equal fitness as those that experienced relaxed competition. Our study suggests that alternative reproductive tactics such as egg dumping can help overcome the frequency-dependent costs of being highly selective in a monogamous mating system, thereby facilitating the evolution of female choosiness.

evolutionary biology↗

bioRxiv2021

Still no evidence for disruption of global patterns of nest predation in shorebirds

Many shorebird species are rapidly declining (Piersma et al. 2016; Munro 2017; Studds et al. 2017), but it is not always clear why. Deteriorating and disappearing habitat, e.g. due to intensive agriculture (Donal et al. 2001; Kentie et al. 2013; Kentie et al. 2018), river regulation (Nebel et al. 2008) or mudflat reclamation (Ma et al. 2014; Larson 2017), and hunting (Reed et al. 2018; Gallo-Cajiao et al. 2020) are some of the documented causes. A recent study suggests yet another possible cause of shorebird decline: a global increase in nest predation (Kubelka et al. 2018). The authors compiled an impressive dataset on patterns of nest predation in shorebirds and their analyses suggest that global patterns of nest predation have been disrupted by climate change, particularly in the Arctic. They go as far as to conclude that the Arctic might have become an ecological trap (Kubelka et al. 2018). Because these findings might have far-reaching consequences for conservation and related political decisions, we scrutinized the study and concluded that the main conclusions of Kubelka et al. (2018) are invalid (Bulla et al. 2019a). The authors then responded by reaffirming their conclusions (Kubelka et al. 2019b). Here, we evaluate some of Kubelka et al.s (2019b) responses, including their recent erratum (2020), and show that the main concerns about the original study still hold. Specifically, (1) we reaffirm that Kubelka et al.s (2018) original findings are confounded by study site. Hence, their conclusions are over-confident because of pseudo-replication. (2) We reiterate that there is no statistical support for the assertion that predation rate has changed in a different way in the Arctic compared to other regions. The relevant test is an interaction between a measure of time (year or period) and a measure of geography (e.g., Arctic vs the rest of the world). The effect of such an interaction is weak, uncertain and statistically non-significant, which undermines Kubelka et al.s (2018) key conclusion. (3) We further confirm that the suggested general increase in predation rates over time is at best a weak and uncertain trend. The most parsimonious hypothesis for the described results is that the temporal changes in predation rate are an artefact of temporal changes in methodology and data quality. Using only high-quality data, i.e. directly calculated predation rates, reveals no overall temporal trend in predation rate. Below we elaborate in detail on each of these points. We conclude that (i) there is no evidence whatsoever that the pattern in the Arctic is different from that in the rest of the world and (ii) there is no solid evidence for an increase in predation rate over time. While we commend Kubelka et al. for compiling and exploring the data, we posit that the data underlying their study, and perhaps all currently available data, are not sufficient (or of sufficient quality) to test their main hypotheses. We call for standardized and consistent data collection protocols and experimental validation of current methods for estimating nesting success.

ecology↗

bioRxiv2021

Machine learning reveals cryptic dialects that guide mate choice in a songbird

Culturally transmitted communication signals - such as human language or bird song - can change over time through a process of cultural drift, and may consequently enhance the separation of populations, potentially leading to reproductive isolation1-4. Local song dialects have been identified in bird species with relatively simple songs where individuals show high cultural conformity5-10. In contrast, the emergence of cultural dialects has been regarded as unlikely11-13 for species with more variable song, such as the zebra finch (Taeniopygia guttata). Instead, it has been proposed that selection for individual recognition and distinctiveness may lead to a complete spread across the space of acoustic and syntactical possibilities11-15. However, another possibility is that analytical limitations have meant that subtle but possibly salient group differences have not yet been discovered in such species. Here we show that machine learning can distinguish the songs from multiple captive zebra finch populations with remarkable precision, and that these cryptic song dialects drive strong assortative mating in this species. We studied mating patterns across three consecutive generations using captive populations that have evolved in isolation for about 100 generations. Cross-fostering eggs within and between these populations and quantifying social interactions of the resulting offspring later in life revealed that mate choice primarily targets cultural traits that are transmitted during a short developmental time window. Detailed social networks showed that females preferentially approached males whose song resembled that of their adolescent peers. Our study shows that birds can be surprisingly sensitive to cultural traits for mating that have hitherto remained cryptic, even in this well-studied species that is used as a model for song-learning13,14,16-28.

animal behavior and cognition↗

bioRxiv2021

Occasional paternal inheritance of the germline-restricted chromosome in songbirds

All songbirds have one special accessory chromosome1-4, the so-called germline-restricted chromosome (GRC)4-7, which is only present in germline cells and absent from all somatic tissues. Earlier work on the zebra finch (Taeniopygia guttata castanotis) showed that the GRC is inherited only through the female line4,6,8,9 - like mitochondrial DNA7,9-12 - and is eliminated from the sperm during spermatogenesis5,7,9-11. Here we show that the GRC can also be paternally inherited. Confocal microscopy using GRC-specific FISH probes indicated that a considerable fraction of sperm heads (1-19%) in zebra finch ejaculates still contained the GRC. In line with these cytogenetic data, sequencing of ejaculates revealed that individual males from two families differed strongly and consistently in the number of GRCs in their ejaculates. Examining a captive-bred population of hybrids of the two zebra finch subspecies (T. g. guttata and T. g. castanotis) revealed that the descendants inherited their mitochondria from a castanotis mother but their GRC from a guttata father. Moreover, GRC haplotypes across nine different castanotis matrilines showed at best a weak tendency to be co-inherited with mtDNA haplotypes. Within castanotis, the GRC showed little variability, while the mtDNA of matrilines was highly divergent. This suggests that a single GRC haplotype has recently spread across the entire castanotis population, crossing the matriline boundaries via paternal spillover. Our findings raise the possibility that certain GRC haplotypes could selfishly spread through the population, via additional paternal transmission, thereby outcompeting other GRC haplotypes that were limited to strict maternal inheritance, even if this was partly detrimental to organismal fitness.

genomics↗

bioRxiv2020

Bird populations most exposed to climate change are less responsive to climatic variation

The phenology of many species shows strong sensitivity to climate change; however, with few large scale intra-specific studies it is unclear how such sensitivity varies over a species range. We document large intra-specific variation in phenological sensitivity to temperature using laying date information from 67 populations of two European songbirds covering a large part of their breeding range. Populations inhabiting deciduous habitats showed stronger phenological sensitivity compared with those in evergreen and mixed habitats. Strikingly, however, the lowest sensitivity was seen in populations that had experienced the greatest change in climate. Therefore, we predict that the strongest phenological advancement will not occur in those populations with the highest sensitivity. Our results show that to effectively assess the impact of climate change on phenology across a species range it will be necessary to account for intra-specific variation in phenological sensitivity, climate change exposure, and the ecological characteristics of a population.

ecology↗

bioRxiv2020

A global analysis of song frequency in passerines provides no support for the acoustic adaptation hypothesis but suggests a role for sexual selection

Many animals use acoustic signals for communication, implying that the properties of these signals can be under strong selection. The acoustic adaptation hypothesis predicts that species living in dense habitats emit lower-frequency sounds than those in open areas, because low-frequency sounds generally propagate further in denser vegetation. Signal frequency may also be under sexual selection, because it correlates with body size and lower-frequency sounds are perceived as more intimidating. Here, we evaluate these hypotheses by analysing variation in peak song frequency across 5,085 passerine species (Passeriformes). A phylogenetically-informed analysis revealed that song frequency decreases with increasing body mass and with male-biased sexual size dimorphism. However, we found no support for the predicted relationship between frequency and habitat. Our results suggest that the global variation in passerine song frequency is mostly driven by natural and sexual selection causing evolutionary shifts in body size rather than by habitat-related selection on sound propagation. Statement of authorshipTA and PM conceived and designed the study with input from all authors. TA and BK coordinated the study. PM collected the song data. MV performed the statistical analyses with input from WF. MB made the figures with help from MV and PM. TP and HB provided bioacoustic expertise. PM drafted the first version of the manuscript. TA, BK and PM revised and finalized the manuscript with input from all authors. Data availability statementThe data used in this study were collected from publicly available databases. All data and computer code used to generate the results, as well as supplementary figures and tables will be freely available at https://osf.io/fa9ky/.

evolutionary biology↗

bioRxiv2020

Body size and climate as predictors of plumage colouration and sexual dichromatism in parrots

Psittaciformes (parrots, cockatoos and lorikeets) comprise one of the most colourful clades of birds. Their unique pigments and cavity nesting habits are two potential explanations for their colourful character. However, plumage colour varies substantially between parrot species and sometimes also between males and females of the same species. Here, we use comparative analyses to evaluate what factors correlate with colour elaboration, colour diversity and sexual dichromatism. Specifically, we test the association between different aspects of parrot colouration and (1) the intensity of sexual selection and social interactions, (2) variation along the slow-fast life-history continuum and (3) climatic variation. We show that larger species and species that live in warm environments display more elaborated colours, yet smaller species have higher levels of sexual dichromatism. Larger parrots tend to have darker and more blue and red colours. Parrots that live in humid environments are darker and redder, whilst species inhabiting warm regions have more blue plumage colours. In general, the variables we considered explain small to moderate amounts of variation in parrot colouration (up to 20%). Our data suggest that sexual selection may be acting more strongly on males in small, short-lived parrots leading to sexual dichromatism. More elaborate colouration in both males and females of the larger, long-lived species with slow tropical life-histories suggests that mutual mate choice and reduced selection for crypsis may be important in these species, as has been shown for passerines.

evolutionary biology↗

bioRxiv2020

Offspring performance is well buffered against stress experienced by ancestors

Evolution should render individuals resistant to stress and particularly to stress experienced by ancestors. However, many studies report negative effects of stress experienced by one generation on the performance of subsequent generations. To assess the strength of such transgenerational effects we used a strategy aimed at overcoming the problem of type I errors when testing multiple proxies of stress in multiple ancestors against multiple offspring performance traits, and applied it to a large observational data set on captive zebra finches (Taeniopygia guttata). We combined clear one-tailed hypotheses with steps of validation, meta-analytic summary of mean effect sizes, and independent confirmatory testing. With this approach we assess to what extent offspring performance in adulthood depends on (1) direct effects of own experiences during early development, (2) indirect condition-transfer effects of the early environment experienced by the parents and the grandparents, and (3) beneficial effects of a match between the environments experienced by the offspring and by its parents. Our study shows that drastic differences in early growth conditions (nestling body mass 8 days after hatching varied 7-fold between 1.7 and 12.4 gram) had only moderate direct effects on adult morphology (95%CI: r=0.19-0.27) and small direct effects on fitness traits (r=0.02-0.12). In contrast, we found no indirect effects of parental or grandparental condition (r=-0.017-0.002; meta-analytic summary of 138 effect sizes), and mixed evidence for small benefits of matching environments, as the latter was not robust to confirmatory testing in independent data sets. This study shows that evolution has led to a remarkable robustness of zebra finches against undernourishment and that transgenerational effects are absent. Author SummaryHow the early life conditions of your ancestors might influence your own life, an aspect of epigenetic inheritance, has become a popular topic among evolutionary biologists and has sparked much interest by the general public. Many theoretical and empirical studies have addressed this question, leading to theories of adaptive programming and condition transfer and ideas of epigenetic or genetic organization. Despite the popularity of this topic, however, there is a lack of a standard framework to guide empirical studies, which are at risk of over-interpreting the most significant effects that might emerge by chance alone when conducting a large number of tests. In this study, we used long-term observational data on multiple morphological and life-history traits of hundreds of male and female zebra finches with information on the early life conditions of both the focal birds and their parents and grandparents. This allows us to comprehensively quantify the magnitude of direct and transgenerational effects of early developmental conditions. Our study (1) proposes a standardized statistical framework for future investigations, (2) summarizes the average effect size (in zebra finches) and indicates the sample sizes needed to pick up such an effect, and (3) provides a counter statement to a growing faith in the ubiquity of transgenerational effects despite their limited evolutionary or mechanistic plausibility.

evolutionary biology↗

bioRxiv2019

Proximate causes of infertility and embryo mortality in captive zebra finches

AbstractSome species show high rates of reproductive failure, which is puzzling because natural selection works against such failure in every generation. Hatching failure is common in both captive and wild zebra finches (Taeniopygia guttata), yet little is known about its proximate causes. Here we analyze data on reproductive performance (fate of >23,000 eggs) based on up to 14 years of breeding of four captive zebra finch populations. We find that virtually all aspects of reproductive performance are negatively affected by inbreeding (mean r = -0.117), by an early-starting, age-related decline (mean r = -0.132), and by poor early-life nutrition (mean r = - 0.058). However, these effects together explain only about 3% of the variance in infertility, offspring mortality, fecundity and fitness. In contrast, individual repeatability of different fitness components varied between 15% and 50%. As expected, we found relatively low heritability in fitness components (median: 7% of phenotypic, and 29% of individually repeatable variation). Yet, some of the heritable variation in fitness appears to be maintained by antagonistic pleiotropy (negative genetic correlations) between male fitness traits and female and offspring fitness traits. The large amount of unexplained variation suggests a potentially important role of local dominance and epistasis, including the possibility of segregating genetic incompatibilities.

evolutionary biology↗

bioRxiv2019

A sex chromosome inversion is associated with copy number variation of mitochondrial DNA in zebra finch sperm

Propulsion of sperm cells via movement of the flagellum is of vital importance for successful fertilization. Presumably, the energy for this movement comes from the mitochondria in the sperm midpiece. Larger midpieces may contain more mitochondria, which should enhance the energetic capacity and hence promote mobility. Due to an inversion polymorphism on their sex chromosome TguZ, zebra finches (Taeniopygia guttata castanotis) exhibit large within-species variation in sperm midpiece length, and those sperm with the longest midpieces swim the fastest. Here, we test through quantitative real-time PCR in zebra finch ejaculates whether the inversion genotype has an effect on the copy number of mitochondrial DNA. Taking the inversion genotype as a proxy for midpiece length, we find that zebra finches with longer midpieces indeed have more copies of the mitochondrial DNA in their ejaculates than those with shorter midpieces, with potential downstream effects on the rate of ATP production and sperm swimming speed. This study sheds light on the proximate cause of a fitness-relevant genetic polymorphism, suggesting the involvement of central components of gamete energy metabolism.\n\nData availabilitySupplementary data file

evolutionary biology↗