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Cosgrove, E. J.

Publications and source records attributed to Cosgrove, E. J..

8 recordsLinked to original sources

Female genetic variation controlling timing of mating plug ejection in Drosophila melanogaster

In multiply-mating species, male-female postcopulatory, prezygotic interactions can influence reproductive outcomes. In Drosophila melanogaster, females can bias sperm storage and usage and thereby influence paternity outcomes. One mechanism by which females may regulate paternity contributions from specific males is through modulation of mating plug ejection timing. The D. melanogaster mating plug is composed of seminal fluid proteins, and some female-derived proteins, that coagulate in the female reproductive tract during mating. The mating plug facilitates sperm storage; thus, timing of female mating plug ejection is associated with sperm storage and relative paternity contributions in cases of multiple mating. However, whether there is natural genetic variation among females that shapes mating plug ejection timing, and genes or phenomena that might mediate it are unknown. We examined mating plug ejection in females from 69 lines of the Drosophila Genetic Reference Panel and observed dramatic differences in median plug ejection timing ranging from less than 1 to over 6 hours. We used this variation to perform a genome-wide association study to identify gene candidates associated with this phenotype. Many gene candidates are expressed in the brain and/or function in neurodevelopment. The candidate pool was also enriched for genes expressed in the ovary and functioning in oogenesis, indicating a link between female reproductive physiology and mating plug ejection. Consistent with this interpretation, females without a germline delay mating plug ejection. Our results demonstrate that female mating plug ejection is a physiologically integrated reproductive trait with a genetic basis that can be shaped by selection. Article SummaryThe D. melanogaster mating plug is composed of seminal fluid proteins and some female-derived proteins that coagulate in the female reproductive tract during mating. The mating plug facilitates sperm storage; thus, timing of female mating plug ejection is associated with sperm storage and relative paternity contributions in cases of multiple mating. Using the DGRP, we observed heritable genetic variation in female timing of mating plug ejection and through a GWAS find associated gene candidates. Gene candidates are enriched for neurodevelopment function and oogenesis function. We experimentally validate the connection between female mating plug ejection and the ovary.

genetics↗

Sustained multigenerational fitness benefits of natural immigration

The fitness of immigrants and their descendants determines the effectiveness of gene flow. Genetic incompatibilities or outbreeding depression can limit the spread of novel alleles, while highly fit immigrant lineages can hasten introgression. These fitness effects of gene flow can also differ between generations as immigrant and resident haplotypes recombine. Understanding the genetic factors that shape immigrant fitness over multiple generations is increasingly important as habitat fragmentation threatens populations by reducing genetic variation and leading to increased levels of inbreeding. Few studies have measured the multigenerational fitness of immigrant lineages, especially within populations that had histories of high gene flow. We used 33 years of life history and pedigree data on a population of Florida scrub-jays (Aphelocoma coerulescens) with historically high immigration to quantify the fitness of immigrants and their descendants. We compared the fitness of immigrants and residents as well as their resulting descendants (F1, F2, etc.) to determine the composite genetic effects responsible for fitness differences. We found evidence of additive benefits of immigrant ancestry and heterosis driven by non-additive effects that persists for multiple generations. These results are promising for conservation efforts aiming to increase connectivity and illustrate the complex dynamics that determine the rates of introgression in natural populations.

evolutionary biology↗

Genome-wide associations of fitness components reveal antagonistic pleiotropy and sexual conflict in the Florida Scrub-Jay

Natural populations often exhibit substantial genetic variation in fitness-related traits, providing the raw material for adaptation. The persistence of high levels of genetic variation in the presence of genetic drift and directional selection has long puzzled evolutionary biologists1-3. Recent studies suggest that antagonistic pleiotropy may play a greater role than previously appreciated, highlighting the need for more empirical studies that consider both sexual antagonism and life-history trade-offs4. Here, we performed a comprehensive assessment of fitness trade-offs within and between sexes in an extensively monitored natural population of Florida Scrub-Jays (Aphelocoma coerulescens)5. We found significant additive genetic variance for female fitness and identified several loci associated with variation in survival, fecundity, and lifetime reproductive success. Many loci associated with multiple fitness components had antagonistic effects, particularly within males. Considering genome-wide polygenic effects, we found multiple genetic trade-offs both within and between sexes, especially when considering different fitness components between sexes. Comparing allele frequency trajectories for putatively pleiotropic loci demonstrated that antagonistic SNPs had smaller allele frequency changes than concordant SNPs. Our fine-scale dissection of fitness components reveals substantial antagonistic pleiotropy that affects short-term evolution, highlighting the importance of antagonistic selection in maintaining genetic variation over short time scales in nature.

evolutionary biology↗

Context-Dependent Fitness Outcomes of Helping in the Cooperatively-Breeding Florida Scrub-Jay (Aphelocoma coerulescens)

Cooperatively breeding species frequently live in family groups of related individuals, with helpers delaying their own reproduction and participating in alloparental care, predator vigilance, and territory defense. It remains challenging to disentangle the roles of the indirect fitness benefits of helping kin and the potential direct fitness benefits helpers receive in the evolution of cooperative breeding. While many studies test for associations between helper relatedness and helping effort, few estimate the realized fitness consequences of helping in relation to these factors. Understanding these fitness outcomes elucidates the selective forces that maintain helping behavior, whether through inclusive fitness gains by helping related individuals or as a means of gaining access to later direct fitness benefits. Using 29 years of extensive demographic data from a closely monitored population of Florida scrub-jays (Aphelocoma coerulescens), we quantified the effect of helpers on breeder survival, offspring survival, and nestling production and how these effects depend on relatedness and sex of helpers. We found that female breeder survival was significantly greater when more helpers were present and that offspring survival was greater when more male helpers were present on small territories. Neither effect of helpers depended on the relatedness between helpers and the individuals they helped. Our results suggest that helping behavior is highly context-dependent and varies based on the potential impact of helping and the direct fitness benefits helpers receive.

ecology↗

Whole-genome sequencing across space and time reveals impact of population decline and reduced gene flow in Florida Scrub-Jays

Whole-genome sequence data is proving to be highly informative about the past demography of free-living populations, and in the context of endangered species, it can provide a quantification of the genetic risk posed by reduced genetic diversity and inbreeding. Prior to 1920, the Florida scrub-jay (Aphelocoma coerulescens) had been widespread across Florida, but with the expansion of agriculture and human habitation, its population has declined by 95%, resulting in fragmentation into semi-isolated subpopulations. By sequencing 241 individuals sampled from five different regions and across two time points, this study quantifies a greater magnitude of loss of genetic diversity and greater levels of inbreeding in smaller and more isolated subpopulations. Consistent with population genetics theory, reduction in population size results in a dramatic loss of rare alleles, skewing the site frequency spectrum far from the expected equilibrium. Increased inbreeding in the smaller, more remote subpopulations is especially evident in the increased size and number of runs of homozygosity. The Florida scrub-jay displays limited dispersal, and habitat fragmentation has greatly reduced the magnitude of gene flow in the past 30 years, resulting in further decline of genetic diversity, especially in the peripheral populations. Analysis of these data is informative in guiding conservation efforts to retain genetic diversity and minimize the consequences of inbreeding in the Florida scrub-jay. HighlightsO_LIFive regional populations show distinct degrees of population isolation and decline. C_LIO_LIThere has been commensurate loss of genetic diversity, skewed site frequency spectra, reduced migration, and increased inbreeding (FROH). C_LIO_LIAs many state-wide populations decline, the smaller, more remote populations provide a glimpse into the future and a testbed for remediation approaches. C_LI

genomics↗

Lifetime fitness benefits of breeding site fidelity and low costs of inbreeding permit inbreeding tolerance in an avian cooperative breeder

Breeding with relatives often decreases individual fitness but can be mitigated via inbreeding avoidance mechanisms such as dispersal, mate-switching, and kin avoidance. Disentangling the effects of multiple mechanisms is challenging without detailed individual-level data and incomplete without considering all life stages. We leveraged 32 years of data from a population of Florida Scrub-Jays (Aphelocoma coerulescens) to investigate how dispersal and mate choice contribute to inbreeding risk across individuals lifetimes and quantify the associated fitness outcomes. We find that when mating is random, inbreeding is two-fold higher when dispersal is limited, but adding sex-biased dispersal significantly reduces inbreeding risk. Limited movement away from the breeding territory for later pairings (site fidelity) contributes more to higher-than-expected levels of inbreeding than limited natal dispersal. Within observed dispersal constraints, however, inbreeding is lower than expected under random mating, suggesting Florida Scrub-Jays actively avoid mating with relatives, especially first-order kin. Finally, males paired with close relatives and females who move farther for later pairings experience equivalently lower lifetime reproductive success. Breeders who move farther for first pairings have lower survival. Overall, our results show how variation in fitness tradeoffs and mate choice behavior across life stages affects inbreeding in a long-lived, social species.

animal behavior and cognition↗

Allele frequency dynamics under sex-biased demography and sex-specific inheritance in a pedigreed population

Sex-biased demography, including sex-biased survival or migration, can alter allele frequency changes across the genome. In particular, we can expect different patterns of genetic variation on autosomes and sex chromosomes due to sex-specific differences in life histories, as well as differences in effective population size, transmission modes, and the strength and mode of selection. Here, we demonstrate the role that sex differences in life history played in shaping short-term evolutionary dynamics across the genome. We used a 25-year pedigree and genomic dataset from a long-studied population of Florida Scrub-Jays (Aphelocoma coerulescens) to directly characterize the relative roles of sex-biased demography and inheritance in shaping genome-wide allele frequency trajectories. We used gene dropping simulations to estimate individual genetic contributions to future generations and to model drift and immigration on the known pedigree. We quantified differential expected genetic contributions of males and females over time, showing the impact of sex-biased dispersal in a monogamous system. Due to female-biased dispersal, more autosomal variation is introduced by female immigrants. However, due to male-biased transmission, more Z variation is introduced by male immigrants. Finally, we partitioned the proportion of variance in allele frequency change through time due to male and female contributions. Overall, most allele frequency change is due to variance in survival and births. Males and females make similar contributions to autosomal allele frequency change, but males make higher contributions to allele frequency change on the Z chromosome. Our work shows the importance of understanding sex-specific demographic processes in characterizing genome-wide allele frequency change in wild populations.

evolutionary biology↗

Allele frequency dynamics in a pedigreed natural population

A central goal of population genetics is to understand how genetic drift, natural selection, and gene flow shape allele frequencies through time. However, the actual processes underlying these changes - variation in individual survival, reproductive success, and movement - are often difficult to quantify. Fully understanding these processes requires the population pedigree, the set of relationships among all individuals in the population through time. Here, we use extensive pedigree and genomic information from a long-studied natural population of Florida Scrub-Jays (Aphelocoma coerulescens) to directly characterize the relative roles of different evolutionary processes in shaping patterns of genetic variation through time. We performed gene dropping simulations to estimate individual genetic contributions to the population and model drift on the known pedigree. We found that observed allele frequency changes are generally well predicted by accounting for the different genetic contributions of founders. Our results show that the genetic contribution of recent immigrants is substantial, with some large allele frequency shifts that otherwise may have been attributed to selection actually due to gene flow. We identified a few SNPs under directional short-term selection after appropriately accounting for gene flow. Using models that account for changes in population size, we partitioned the proportion of variance in allele frequency change through time. Observed allele frequency changes are primarily due to variation in survival and reproductive success, with gene flow making a smaller contribution. This study provides one of the most complete descriptions of short-term evolutionary change in allele frequencies in a natural population to date.

evolutionary biology↗