BMC Evolutionary Biology

Gene duplication and an accelerated evolutionary rate in 11S globulin genes are associated with higher protein synthesis in dicots as compared to monocots.

Publication Date: 2012 Jan 31 PMID: 22292855
Authors: Li, C. - Li, M. - Dunwell, J. M. - Zhang, Y. M.
Journal: BMC Evol Biol

ABSTRACT: BACKGROUND: Seed storage proteins are a major source of dietary protein, and the content of such proteins determines both the quantity and quality of crop yield. Significantly, examination of the protein content in the seeds of crop plants shows a distinct difference between monocots and dicots. Thus, it is expected that there are different evolutionary patterns in the genes underlying protein synthesis in the seeds of these two groups of plants. RESULTS: Gene duplication, evolutionary rate and positive selection of a major gene family of seed storage proteins (the 11S globulin genes), were compared in dicots and monocots. The results, obtained from five species in each group, show more gene duplications, a higher evolutionary rate and positive selections of this gene family in dicots, which are rich in 11S globulins, but not in the monocots. CONCLUSION: Our findings provide evidence to support the suggestion that gene duplication and an accelerated evolutionary rate may be associated with higher protein synthesis in dicots as compared to monocots.

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Evolutionary history of the genus Tarentola (Gekkota: Phyllodactylidae) from the Mediterranean Basin, estimated using multilocus sequence data.

Publication Date: 2012 Jan 30 PMID: 22289419
Authors: Rato, C. - Carranza, S. - Harris, D. J.
Journal: BMC Evol Biol

ABSTRACT: BACKGROUND: The pronounced morphological conservatism within Tarentola geckos contrasted with a high genetic variation in North Africa, has led to the hypothesis that this group could represent a cryptic species complex, a challenging system to study especially when trying to define distinct evolutionary entities and address biogeographic hypotheses. In the present work we have re-examined the phylogenetic and phylogeographic relationships between and within all Mediterranean species of Tarentola, placing the genealogies obtained into a temporal framework. In order to do this, we have investigated the sequence variation of two mitochondrial (12S rRNA and 16S rRNA), and four nuclear markers (ACM4, PDC, MC1R, and RAG2) for 384 individuals of all known Mediterranean Tarentola species, so that their evolutionary history could be assessed. RESULTS: Of all three generated genealogies (combined mtDNA, combined nDNA, and mtDNA+nDNA) we prefer the phylogenetic relationships obtained when all genetic markers are combined. A total of 133 individuals, and 2,901 bp of sequence length, were used in this analysis. The phylogeny obtained for Tarentola presents deep branches, with T. annularis, T. ephippiata and T. chazaliae occupying a basal position and splitting from the remaining species around 15.38 Mya. Tarentola boehmei is sister to all other Mediterranean species, from which it split around 11.38 Mya. There are also two other major groups: 1) the T. mauritanica complex present in North Africa and Europe; and 2) the clade formed by the T. fascicularis/deserti complex, T. neglecta and T. mindiae, occurring only in North Africa. The cladogenesis between these two groups occurred around 8.69 Mya, coincident with the late Miocene. Contrary to what was initially proposed, T. neglecta and T. mindiae are sister taxa to both T. fascicularis and T. deserti. CONCLUSIONS: At least in the Iberian Peninsula and Northwest Africa, the lineages obtained have some geographic coherency, whilst the evolutionary history of the forms from Northeast Africa remains unclear, with a paraphyletic T. fascicularis with respect to T. deserti. The separation between the T. mauritanica complex and the clade formed by the T. fascicularis/deserti complex, T. neglecta and T. mindiae is coincident with the uplift of the Atlas Mountain chain, and the establishment of two distinct bioclimatic regions on each side of the barrier.

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The evolutionary history of protein fold families and proteomes confirms that the archaeal ancestor is more ancient than the ancestors of other superkingdoms.

Publication Date: 2012 Jan 27 PMID: 22284070
Authors: Kim, K. M. - Caetano-Anolles, G.
Journal: BMC Evol Biol

ABSTRACT: BACKGROUND: The entire evolutionary history of life can be studied using myriad sequences generated by genomic research. This includes the appearance of the first cells and of superkingdoms Archaea, Bacteria, and Eukarya. However, the use of molecular sequence information for deep phylogenetic analyses is limited by mutational saturation, differential evolutionary rates, lack of sequence site independence, and other biological and technical constraints. In contrast, protein structures are evolutionary modules that are highly conserved and diverse enough to enable deep historical exploration. RESULTS: Here we build phylogenies that describe the evolution of proteins and proteomes. These phylogenetic trees are derived from a genomic census of protein domains defined at the fold family (FF) level of structural classification. Phylogenomic trees of FF structures were reconstructed from genomic abundance levels of 2,397 FFs in 420 proteomes of free-living organisms. These trees defined timelines of domain appearance, with time spanning from the origin of proteins to the present. Timelines are divided into five different evolutionary phases according to patterns of sharing of FFs among superkingdoms: (1) a primordial protein world, (2) reductive evolution and the rise of Archaea, (3) the rise of Bacteria from the common ancestor of Bacteria and Eukarya and early development of the three superkingdoms, (4) the rise of Eukarya and widespread organismal diversification, and (5) eukaryal diversification. The relative ancestry of the FFs shows that reductive evolution by domain loss is dominant in the first three phases and is responsible for both the diversification of life from a universal cellular ancestor and the appearance of superkingdoms. On the other hand, domain gains are predominant in the last two phases and are responsible for organismal diversification, especially in Bacteria and Eukarya. CONCLUSIONS: The evolution of functions that are associated with corresponding FFs along the timeline reveals that primordial metabolic domains evolved earlier than informational domains involved in translation and transcription, supporting the metabolism-first hypothesis rather than the RNA world scenario. In addition, phylogenomic trees of proteomes reconstructed from FFs appearing in each of the five phases of the protein world show that trees reconstructed from ancient domain structures were consistently rooted in archaeal lineages, supporting the proposal that the archaeal ancestor is more ancient than the ancestors of other superkingdoms.

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Fine-scale temporal and spatial variation of taxon and clonal structure in the Daphnia longispina hybrid complex in heterogeneous environments.

Publication Date: 2012 Jan 27 PMID: 22280487
Authors: Yin, M. - Petrusek, A. - Seda, J. - Wolinska, J.
Journal: BMC Evol Biol

ABSTRACT: BACKGROUND: Cyclical parthenogenetic water fleas of the genus Daphnia have become a prominent model organism in ecology and evolution. In the past, analyses of their population structure have been limited by the prevailing use of allozyme markers, which in general do not allow for the distinction of individual clones. In this study, we used 10 microsatellite markers to track changes in the taxonomic and clonal composition of Daphnia populations, and traced the abundance of the most common clones in two European reservoirs. One of the localities was inhabited by a single species of the Daphnia longispina complex (D. galeata), the other by two parental species (D. galeata and D. longispina) and their interspecific hybrids. The study took place during the transition from summer stratification to autumn mixing, representing a period of major environmental change within lake habitats. RESULTS: In both reservoirs, we observed temporal (generation-to-generation) and spatial (along the heterogeneous reservoir environment) changes in Daphnia community structure. In the single-species reservoir, the clonal diversity of D. galeata increased with time, as a few dominant clones were replaced by a higher number of less common clones. A loss in selective advantage for the dominant clones may have been due to gradual changes in the environment, or due to selection acting in a negative frequency-dependent manner. In the multispecies reservoir, there were no apparent temporal trends in clonal diversity but we observed significantly lower clonal diversity in the interspecific hybrids than in the coexisting parental species, supporting the existence of reproductive barriers between the parental genomes. CONCLUSIONS: Our study, tracing clonal lineages of Daphnia in time and space by the fine-resolution markers, contributes to the understanding of how clonal reproduction impacts community structure in cyclically parthenogenetic organisms.

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Complex adaptive responses during antagonistic coevolution between Tribolium castaneum and its natural parasite Nosema whitei revealed by multiple fitness components.

Publication Date: 2012 Jan 26 PMID: 22280468
Authors: Berenos, C. - Schmid-Hempel, P. - Wegner, K. M.
Journal: BMC Evol Biol

ABSTRACT: BACKGROUND: Host-parasite coevolution can lead to local adaptation of either parasite or host if there is specificity (GxG interactions) and asymmetric evolutionary potential between host and parasite. This has been demonstrated both experimentally and in field studies, but a substantial proportion of studies fail to detect such clear-cut patterns. One explanation for this is that adaptation can be masked by counter-adaptation by the antagonist. Additionally, genetic architecture underlying the interaction is often highly complex thus preventing specific adaptive responses. Here, we have employed a reciprocal cross-infection experiment to unravel the adaptive responses of two components of fitness affecting both parties with different complexities of the underlying genetic architecture (i.e. mortality and spore load). Furthermore, our experimental coevolution of hosts (Tribolium castaneum) and parasites (Nosema whitei) included paired replicates of naive hosts from identical genetic backgrounds to allow separation between host- and parasite-specific responses. RESULTS: In hosts, coevolution led to higher resistance and altered resistance profiles compared to paired control lines. Host genotype x parasite genotype interactions (GH x GP) were observed for spore load (the trait of lower genetic complexity), but not for mortality. Overall parasite performance correlated with resistance of its matching host coevolution background reflecting a directional and unspecific response to strength of selection during coevolution. Despite high selective pressures exerted by the obligatory killing parasite, and host- and parasite-specific mortality profiles, no general pattern of local adaptation was observed, but one case of parasite maladaptation was consistently observed on both coevolved and control host populations. In addition, the use of replicate control host populations in the assay revealed one case of host maladaptation and one case of parasite adaptation that was masked by host counter-adaptation, suggesting the presence of complex and probably dynamically changing fitness landscapes. CONCLUSIONS: Our results demonstrate that the use of replicate naive populations can be a useful tool to differentiate between host and parasite adaptation in complex and dynamic fitness landscapes. The absence of clear local adaptation patterns during coevolution with a sexual host showing a complex genetic architecture for resistance suggests that directional selection for generality may be more important attributes of host-parasite coevolution than commonly assumed.

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Evolutionary Dynamics of Human Autoimmune Disease Genes and Malfunctioned Immunological Genes.

Publication Date: 2012 Jan 25 PMID: 22276655
Authors: Podder, S. - Ghosh, T. C.
Journal: BMC Evol Biol

ABSTRACT: BACKGROUND: One of the main issues of molecular evolution is to divulge the principles in dictating the evolutionary rate differences among various gene classes. Immunological genes have received considerable attention in evolutionary biology as candidates for local adaptation and for studying functionally important polymorphisms. The normal structure and function of immunological genes will be distorted when they experience mutations leading to immunological dysfunctions. RESULTS: Here, we examined the fundamental differences between the genes which on mutation give rise to autoimmune or other immune system related diseases and the immunological genes that do not cause any disease phenotypes. Although the disease genes examined are analogous to non-disease genes in product, expression, function, and pathway affiliation, a statistically significant decrease in evolutionary rate has been found in autoimmune disease genes relative to all other immune related diseases and non-disease genes. Possible ways of accumulation of mutation in the three steps of the central dogma (DNA-mRNA-Protein) have been studied to trace the mutational effects predisposed to disease consequence and acquiring higher selection pressure. Principal Component Analysis and Multivariate Regression Analysis have established the predominant role of single nucleotide polymorphisms in guiding the evolutionary rate of immunological disease and non-disease genes followed by m-RNA abundance, paralogs number, fraction of phosphorylation residue, alternatively spliced exon, protein residue burial and protein disorder. CONCLUSIONS: Our study provides an empirical insight into the etiology of autoimmune disease genes and other immunological diseases. The immediate utility of our study is to help in disease gene identification and may also help in medicinal improvement of immune related disease.

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Gene flow and population structure in the Mexican blind cavefish complex (Astyanax mexicanus).

Publication Date: 2012 Jan 23 PMID: 22269119
Authors: Bradic, M. - Beerli, P. - Garcia-de Leon, F. J. - Esquivel-Bobadilla, S. - Borowsky, R. L.
Journal: BMC Evol Biol

ABSTRACT: BACKGROUND: Cave animals converge evolutionarily on a suite of troglomorphic traits, the best known of which are eyelessness and depigmentation. We studied 11 cave and 10 surface populations of Astyanax mexicanus in order to better understand the evolutionary origins of the cave forms, the basic genetic structuring of both cave and surface populations, and the degree to which present day migration among them affects their genetic divergence. RESULTS: To assess the genetic structure within populations and the relationships among them we genotyped individuals at 26 microsatellite loci. We found that surface populations are similar to one another, despite their relatively large geographic separation, whereas the cave populations are better differentiated. The cave populations we studied span the full range of the cave forms in three separate geographic regions and have at least five separate evolutionary origins. We found lower genetic diversity in cave than in surface populations correlated with their smaller effective population sizes, probably the result of food and space limitations. Some of the cave populations receive migrants from the surface and exchange migrants with one another, especially when geographically close. This admixture results in significant heterozygote deficiencies at numerous loci due to Wahlund effects. Cave populations receiving migrants from the surface contain small numbers of individuals that are intermediate in both phenotype and genotype, affirming at least limited gene flow from the surface. CONCLUSIONS: Cave populations of this species are derived from two different surface stocks denoted "old" and "new." The old stock colonized caves at least three times independently while the new stock colonized caves at least twice independently. Thus, the similar cave phenotypes found in these caves are the result of repeated convergences. These phenotypic convergences have occurred in spite of gene flow from surface populations suggesting either strong natural or sexual selection for alleles responsible for the cave phenotype in the cave environment.

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Slow but not low: genomic comparisons reveals slower evolutionary rate and higher dN/dS in conifers compared to angiosperms.

Publication Date: 2012 Jan 20 PMID: 22264329
Authors: Buschiazzo, E. - Ritland, C. - Bohlmann, J. - Ritland, K.
Journal: BMC Evol Biol

ABSTRACT: BACKGROUND: Comparative genomics can inform us about the processes of mutation and selection across diverse taxa. Among seed plants, gymnosperms have been lacking in genomic comparisons. Recent EST and full-length cDNA collections for two conifers, Sitka spruce (Picea sitchensis) and loblolly pine (Pinus taeda), together with full genome sequences for two angiosperms, Arabidopsis thaliana and poplar (Populus trichocarpa), offer an opportunity to infer the evolutionary processes underlying thousands of orthologous protein-coding genes in gymnosperms compared with an angiosperm orthologue set. RESULTS: Based upon pairwise comparisons of 3,723 spruce and pine orthologues, we found an average synonymous genetic distance (dS) of 0.191, and an average dN/dS ratio of 0.314. Using a fossil-established divergence time of 140 million years between spruce and pine, we extrapolated a nucleotide substitution rate of 0.68 x 10-9 synonymous substitutions per site per year. When compared to angiosperms, this indicates a dramatically slower rate of nucleotide substitution rates in conifers: on average 15-fold. Coincidentally, we found a three-fold higher dN/dS for the spruce-pine lineage compared to the poplar-Arabidopsis lineage. This joint occurrence of a slower evolutionary rate in conifers with higher dN/dS, and possibly positive selection, showcases the uniqueness of conifer genome evolution. CONCLUSIONS: Our results are in line with documented reduced nucleotide diversity, conservative genome evolution and low rates of diversification in conifers on the one hand and numerous examples of local adaptation in conifers on the other hand. We propose that reduced levels of nucleotide mutation in large and long-lived conifer trees, coupled with large effective population size, were the main factors leading to slow substitution rates but retention of beneficial mutations.

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Rates of evolution in stress-related genes are associated to habitat preference in two Cardamine lineages.

Publication Date: 2012 Jan 18 PMID: 22257588
Authors: Ometto, L. - Li, M. - Bresadola, L. - Varotto, C.
Journal: BMC Evol Biol

ABSTRACT: BACKGROUND: Elucidating the selective and neutral forces underlying molecular evolution is fundamental to understanding the genetic basis of adaptation. Plants have evolved a suite of adaptive responses to cope with variable environmental conditions, but relatively little is known about which genes are involved in such responses. Here we studied molecular evolution on a genome-wide scale in two species of Cardamine with distinct habitat preferences: C. resedifolia, found at high altitudes, and C. impatiens, found at low altitudes. Our analyses focussed on genes that are involved in stress responses to two factors that differentiate the high- and low-altitude habitats, namely temperature and irradiation. RESULTS: High-throughput sequencing was used to obtain gene sequences from C. resedifolia and C. impatiens. Using the available A. thaliana gene sequences and annotation, we identified nearly 3,000 triplets of putative orthologues, including genes involved in cold response, photosynthesis or in general stress responses. By comparing estimated rates of molecular substitution, codon usage, and gene expression in these species with those of Arabidopsis, we were able to evaluate the role of positive and relaxed selection in driving the evolution of Cardamine genes. Our analyses revealed a statistically significant higher rate of molecular substitution in C. resedifolia than in C. impatiens, compatible with more efficient positive selection in the former. Conversely, the genome-wide level of selective pressure is compatible with more relaxed selection in C. impatiens. Moreover, levels of selective pressure were heterogeneous between functional classes and between species, with cold responsive genes evolving particularly fast in C. resedifolia, but not in C. impatiens. CONCLUSIONS: Overall, our comparative genomic analyses revealed that differences in effective population size might contribute to the differences in the rate of protein evolution and in the levels of selective pressure between the C. impatiens and C. resedifolia lineages. The within-species analyses also revealed evolutionary patterns associated with habitat preference of two Cardamine species. We conclude that the selective pressures associated with the habitats typical of C. resedifolia may have caused the rapid evolution of genes involved in cold response.

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Evolutionary dynamics of protein domain architecture in plants.

Publication Date: 2012 Jan 17 PMID: 22252370
Authors: Zhang, X. C. - Wang, Z. - Zhang, X. - Le, M. H. - Sun, J. - Xu, D. - Cheng, J. - Stacey, G.
Journal: BMC Evol Biol

ABSTRACT: BACKGROUND: Protein domains are the structural, functional and evolutionary units of the protein. Protein domain architectures are the linear arrangements of domain(s) in individual proteins. Although the evolutionary history of protein domain architecture has been extensively studied in microorganisms, the evolutionary dynamics of domain architecture in the plant kingdom remains largely undefined. To address this question, we analyzed the lineage-based protein domain architecture content in 14 completed green plant genomes. RESULTS: Our analyses show that all 14 plant genomes maintain similar distributions of species-specific, single-domain, and multi-domain architectures. Approximately 65% of plant domain architectures are universally present in all plant lineages, while the remaining architectures are lineage-specific. Clear examples are seen of both the loss and gain of specific protein architectures in higher plants. There has been a dynamic, lineage-wise expansion of domain architectures during plant evolution. The data suggest that this expansion can be largely explained by changes in nuclear ploidy resulting from rounds of whole genome duplications. Indeed, there has been a decrease in the number of unique domain architectures when the genomes were normalized into a presumed ancestral genome that has not undergone whole genome duplications. CONCLUSIONS: Our data show the conservation of universal domain architectures in all available plant genomes, indicating the presence of an evolutionarily conserved, core set of protein components. However, the occurrence of lineage-specific domain architectures indicates that domain architecture diversity has been maintained beyond these core components in plant genomes. Although several features of genome-wide domain architecture content are conserved in plants, the data clearly demonstrate lineage-wise, progressive changes and expansions of individual protein domain architectures, reinforcing the notion that plant genomes have undergone dynamic evolution.

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Molecular evolution of Drosophila Sex-lethal and related sex determining genes.

Publication Date: 2012 Jan 14 PMID: 22244243
Authors: Mullon, C. - Pomiankowski, A. - Reuter, M.
Journal: BMC Evol Biol

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.

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Evolution, expansion and expression of the Kunitz/BPTI gene family associated with long-term blood feeding in Ixodes Scapularis.

Publication Date: 2012 Jan 14 PMID: 22244187
Authors: Dai, S. X. - Zhang, A. D. - Huang, J. F.
Journal: BMC Evol Biol

ABSTRACT: BACKGROUND: Recent studies of the tick saliva transcriptome have revealed the profound role of salivary proteins in blood feeding. Kunitz/BPTI proteins are abundant in the salivary glands of ticks and perform multiple functions in blood feeding, such as inhibiting blood coagulation, regulating host blood supply and disrupting host angiogenesis. However, Kunitz/BPTI proteins in soft and hard ticks have different functions and molecular mechanisms. How these differences emerged and whether they are associated with the evolution of long-term blood feeding in hard ticks remain unknown. RESULTS: In this study, the evolution, expansion and expression of Kunitz/BPTI family in Ixodes scapularis were investigated. Single- and multi-domain Kunitz/BPTI proteins have similar gene structures. Single-domain proteins were classified into three groups (groups I, II and III) based on their cysteine patterns. Group I represents the ancestral branch of the Kunitz/BPTI family, and members of this group function as serine protease inhibitors. The group I domain was used as a module to create multi-domain proteins in hard ticks after the split between hard and soft ticks. However, groups II and III, which evolved from group I, are only present and expanded in the genus Ixodes. These lineage-specific expanded genes exhibit significantly higher expression during long-term blood feeding in Ixodes scapularis. Interestingly, functional site analysis suggested that group II proteins lost the ability to inhibit serine proteases and evolved a new function of modulating ion channels. Finally, evolutionary analyses revealed that the expansion and diversification of the Kunitz/BPTI family in the genus Ixodes were driven by positive selection. CONCLUSIONS: These results suggest that the differences in the Kunitz/BPTI family between soft and hard ticks may be linked to the evolution of long-term blood feeding in hard ticks. In Ixodes, the lineage-specific expanded genes (Group II and III) lost the ancient function of inhibiting serine proteases and evolved new functions to adapt to long-term blood feeding. Therefore, these genes may play a profound role in the long-term blood feeding of hard ticks. Based our analysis, we propose that the six genes identified in our study may be candidate target genes for tick control.

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Mate choice for a male carotenoid-based ornament is linked to female dietary carotenoid intake and accumulation.

Publication Date: 2012 Jan 10 PMID: 22233462
Authors: Toomey, M. B. - McGraw, K. J.
Journal: BMC Evol Biol

ABSTRACT: BACKGROUND: The coevolution of male traits and female mate preferences has led to the elaboration and diversification of sexually selected traits; however the mechanisms that mediate trait-preference coevolution are largely unknown. Carotenoid acquisition and accumulation are key determinants of the expression of male sexually selected carotenoid-based coloration and a primary mechanism maintaining the honest information content of these signals. Carotenoids also influence female health and reproduction in ways that may alter the costs and benefits of mate choice behaviours and thus provide a potential biochemical link between the expression of male traits and female preferences. To test this hypothesis, we manipulated the dietary carotenoid levels of captive female house finches (Carpodacus mexicanus) and assessed their mate choice behavior in response to color-manipulated male finches. RESULTS: Females preferred to associate with red males, but carotenoid supplementation did not influence the direction or strength of this preference. Females receiving a low-carotenoid diet were less responsive to males in general, and discrimination among the colorful males was positively linked to female plasma carotenoid levels at the beginning of the study when the diet of all birds was carotenoid-limited. CONCLUSIONS: Although female preference for red males was not influenced by carotenoid intake, changes in mating responsiveness and discrimination linked to female carotenoid status may alter how this preference is translated into choice. The reddest males, with the most carotenoid rich plumage, tend to pair early in the breeding season. If carotenoid-related variations in female choice behaviour shift the timing of pairing, then they have the potential to promote assortative mating by carotenoid status and drive the evolution of carotenoid-based male plumage coloration.

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