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Abstract Background Changes in gene regulatory networks drive the evolution of phenotypic diversity both within and between species. Rewiring of transcriptional networks is achieved either by changes to transcription factor binding sites or by changes to the physical interactions among transcription factor proteins. It has been suggested that the evolution of cooperative binding among factors can facilitate the adaptive rewiring of a regulatory network. Results We use a population-genetic model to explore when cooperative binding of transcription factors is favored by evolution, and what effects cooperativity then has on the adaptive re-writing of regulatory networks. We consider a pair of transcription factors that regulate multiple targets and overlap in the sets of target genes they regulate. We show that, under stabilising selection, cooperative binding between the transcription factors is favoured provided the amount of overlap between their target genes exceeds a threshold. The value of this threshold depends on several population-genetic factors: strength of selection on binding sites, cost of pleiotropy associated with protein-protein interactions, rates of mutation and population size. Once it is established, we find that cooperative binding of transcription factors significantly accelerates the adaptive rewiring of transcriptional networks under positive selection. We compare our qualitative predictions to systematic data on Saccharomyces cerevisiae transcription factors, their binding sites, and their protein-protein interactions. Conclusions Our study reveals a rich set of evolutionary dynamics driven by a tradeoff between the beneficial effects of cooperative binding at targets shared by a pair of factors, and the detrimental effects of cooperative binding for non-shared targets. We find that cooperative regulation will evolve when transcription factors share a sufficient proportion of their target genes. These findings help to explain empirical pattens in datasets of transcription factors in Saccharomyces cerevisiae and, they suggest that changes to physical interactions between transcription factors can play a critical role in the evolution of gene regulatory networks.

Abstract Background Sex determining mechanisms are evolutionarily labile and related species often use different primary signals and gene regulatory networks. This is well illustrated by the sex determining cascade of Drosophila fruitflies, which have recruited Sex-lethal as the master switch and cellular memory of sexual identity, a role performed in other insects by the gene transformer. Here we investigate the evolutionary change in the coding sequences of sex determining genes associated with the recruitment of Sex-lethal. We analyze sequences of Sex-lethal itself, its Drosophila paralogue sister-or-Sex-lethal and downstream targets transformer and doublesex. Results We find that the recruitment of sister-or-Sex-lethal was associated with a number of adaptive amino acid substitutions, followed by a tightening of purifying selection within the Drosophila clade. Sequences of the paralogue sister-or-Sex-lethal, in contrast, show a signature of rampant positive selection and relaxation of purifying selection. The recruitment of Sex-lethal as top regulator and memory gene is associated with a significant release from purifying selection in transformer throughout the Drosophila clade. In addition, doublesex shows a signature of positive selection and relaxation of purifying selection in the Drosophila clade. A similar pattern is seen in sequences from the sister Tephritidae clade. Conclusions The pattern of molecular evolution we observe for Sex-lethal and its paralogue sister-or-Sex-lethal is not characteristic of a duplication followed by neo-functionalization. Rather, evidence suggests a sub-functionalization scenario achieved through the evolution of sophisticated splicing. As expected, we find that transformer evolves under relaxed purifying selection after the recruitment of Sex-lethal in Drosophila. Finally, the observation of doublesex adaptation in both Drosophila and Tephritidae suggests that these changes are due to ongoing adaptation of downstream sex-specific regulation, rather than being associated the recruitment of Sex-lethal and the resulting change in the topology of the sex determining cascade.

Abstract Background Sex determination networks evolve rapidly and have been studied intensely across many species, particularly in insects, thus presenting good models to study the evolutionary plasticity of gene networks. Results We study the evolution of an unlinked gene capable of regulating an existing diploid sex determination system. Differential gene expression determines phenotypic sex and fitness, dramatically reducing the number of assumptions of previous models. It allows us to make a quantitative evaluation of the full range of evolutionary outcomes of the system and an assessment of the likely contribution of sexual conflict to change in sex determination systems. Our results show under what conditions network mutations causing differential regulation can lead to the reshaping of sex determination networks. Conclusion The analysis demonstrates the complex relationship between mutation and outcome: the same mutation can produce many different evolved populations, while the same evolved population can be produced by many different mutations. Existing network structure alters the constraints and frequency of evolutionary changes, which include the recruitment of new regulators, changes in heterogamety, protected polymorphisms, and transitions to a new locus that controls sex determination.

Abstract When species shift their ranges to track climate change, they are almost certain to experience novel environments to which they are poorly adapted. Otaki and co-workers document an explosion of wing pattern variation accompanying range expansion in the pale grass blue butterfly. This pattern can be replicated in the laboratory using artificial selection on cold shocked pupae, at temperature extremes typical of recently colonized environments. We discuss how this phenotypic plasticity may be associated with successful colonization and how significant local adaptation is likely to re-establish developmental control. Integrating knowledge of trait plasticity into current genetic models of adaptation is central to our understanding of when and where a colonising population will be able to persist and adapt in novel surroundings.

Abstract Background Exaggerated male ornaments and displays often evolve in species where males only provide females with ejaculates during reproduction. Although "good genes" arguments are typically invoked to explain this phenomenon, a simpler alternative is possible if variation in male reproductive quality (e.g. sperm number, ejaculate content, mating rate) is an important determinant of female reproductive success. The "phenotype-linked fertility hypothesis" states that female preference for male ornaments or displays has been selected to ensure higher levels of fertility and has driven the evolution of exaggerated male traits. Females of the stalk-eyed fly Teleopsis dalmanni must mate frequently to maintain high levels of fertility and prefer to mate with males exhibiting large eyespan, a condition-dependent sexual ornament. If eyespan indicates male reproductive quality, females could directly increase their reproductive success by mating with males with large eyespan. Here we investigate whether male eyespan indicates accessory gland and testis length, and then ask whether mating with large eyespan males affects female fertility. Results Male eyespan was a better predictor of two key male reproductive traits – accessory gland and testis length – than was body size alone. This positive relationship held true over three levels of increasing environmental stress during the maturation of the adult accessory glands and testes. Furthermore, females housed with a large eyespan male exhibited higher levels of fertility than those with small eyespan males. Conclusion Male eyespan in stalk-eyed flies is subject to strong directional mate preference and is a reliable indicator of male reproductive quality – both because males with larger eyespan have bigger accessory glands and testes, and also as they confer higher fertility on females. Fertility enhancement may have arisen because males with larger eyespan mated more often and/or because they transferred more sperm or other substances per ejaculate. The need to ensure high levels of fertility could thus have been an important selective force in the coevolution of female preference and male eyespan in stalk-eyed flies. Our results support the phenotype-linked fertility hypothesis and suggest that it might be of general importance in explaining the evolution of exaggerated male ornaments and displays in species where males only provide females with ejaculates during reproduction.

Abstract Background When females mate with different males, competition for fertilizations occurs after insemination. Such sperm competition is usually summarized at the level of the population or species by the parameter, P2, defined as the proportion of offspring sired by the second male in double mating trials. However, considerable variation in P2 may occur within populations, and such variation limits the utility of population-wide or species P2 estimates as descriptors of sperm usage. To fully understand the causes and consequences of sperm competition requires estimates of not only mean P2, but also intra-specific variation in P2. Here we investigate within-population quantitative variation in P2 using a controlled mating experiment and microsatellite profiling of progeny in the multiply mating stalk-eyed fly, Teleopsis dalmanni. Results We genotyped 381 offspring from 22 dam-sire pair families at four microsatellite loci. The mean population-wide P2 value of 0.40 was not significantly different from that expected under random sperm mixing (i.e. P2 = 0.5). However, patterns of paternity were highly variable between individual families; almost half of families displayed extreme second male biases resulting in zero or complete paternity, whereas only about one third of families had P2 values of 0.5, the remainder had significant, but moderate, paternity skew. Conclusion Our data suggest that all modes of ejaculate competition, from extreme sperm precedence to complete sperm mixing, occur in T. dalmanni. Thus the population mean P2 value does not reflect the high underlying variance in familial P2. We discuss some of the potential causes and consequences of post-copulatory sexual selection in this important model species.

Abstract Background Internal reproductive organ size is an important determinant of male reproductive success. While the response of testis length to variation in the intensity of sperm competition is well documented across many taxa, few studies address the importance of testis size in determining other components of male reproductive success (such as mating frequency) or the significance of size variation in accessory reproductive organs. Accessory gland length, but not testis length, is both phenotypically and genetically correlated with male mating frequency in the stalk-eyed fly Cyrtodiopsis dalmanni. Here we directly manipulate male mating status to investigate the effect of copulation on the size of both the testes and the accessory glands of C. dalmanni. Results Accessory gland length was positively correlated with male mating frequency. Copulation induced a significant decrease in accessory gland size. The size of the accessory glands then recovered slowly over the next 8–48 hours. Neither testis length nor testis area was altered by copulation. Conclusion These results reveal that the time course of accessory gland recovery corresponds to field observations of mating behaviour and suggest that accessory gland size may limit male mating frequency in C. dalmanni.