Understanding why organisms vary in developmental plasticity has implications for predicting population responses to changing environments and the maintenance of intraspecific variation. The epiphenotype hypothesis posits that the timing of development can constrain plasticity—the earlier alternate phenotypes begin to develop, the greater the difference that can result amongst the final traits. This research extends this idea by considering how life history timing shapes the opportunity for the environment to influence trait development. We test the prediction that the earlier an individual begins to actively interact with and explore their environment, the greater the opportunity for plasticity and thus variation in foraging traits. This research focuses on life history variation across four groups of birds using museum specimens and measurements from the literature. We reasoned that greater phenotypic plasticity, through either environmental effects or genotype-by-environment interactions in development, would be manifest in larger trait ranges (bills and tarsi) within species. Among shorebirds and ducks, we found that species with relatively shorter incubation times tended to show greater phenotypic variation. Across warblers and sparrows, we found little support linking timing of flight and trait variation. Overall, our results also suggest a pattern between body size and trait variation, consistent with constraints on egg size that might result in larger species having more environmental influences on development. Taken together, our results provide some support for the hypothesis that variation in life histories affects how the environment shapes development, through either the expression of plasticity or the release of cryptic genetic variation.
The East African cichlid fishes provide text book examples of adaptive radiation. Diversification and speciation of cichlids associate with variation in diet and trophic morphologies among other ecological, behavioural and morphological phenotypes (Kocher 2004). Numerous case studies in cichlids reveal a role of developmental plasticity in generating jaw ecomorphs in response to variation in feeding ecology that can facilitate niche exploitation and subsequent diversification (e.g. Meyer 1987). Specifically, genetic divergence among such environmentally induced morphs can occur via reproductive isolation due to divergence in habitat and resource use in combination with genetic assimilation of environmentally induced phenotypes (West-Eberhard 2003; Pfenniget al. 2010). Expansion of this conceptual model has been hampered in part by the limited knowledge of the molecular mechanisms of plasticity in nonstandard model systems and the associated lack of evidence linking the molecular mechanisms of plasticity to those that generate phenotypic divergence among populations and taxa. In this issue of Molecular Ecology, Gunteret al. (2013) identify the transcriptional mechanisms of diet-induced lower pharyngeal jaw (LPJ) plasticity in the cichlid fish Astatoreochromis alluaudi. Natural populations of A. alluaudi exhibit variation in jaw morphology in relation to diet hardness. Among the plastic responses to diet are adjustments to the LPJ ranging from a robust molariform morph in response to a hard diet to a more gracile papilliform morph in response to a soft diet (Fig. 1). Gunter and colleagues induced developmental plasticity of the A. alluaudi jaw using diet manipulations and compared LPJ transcriptomic profiles of the resulting morphs. In this foundational work, the authors identify 187 differentially expressed genes that underlie the development and maintenance of diet-induced LPJ morphologies. This list includes a wide range of genes spanning from broad-acting transcription factors to signalling molecules and structural genes. Here, I examine the ontogeny of the molecular response to mechanical strain imposed by diet hardness and discuss the role of the stages of this response in the evolution of plasticity and plasticity-driven diversification.
Although the morphological and physiological changes involved in pregnancy in live-bearing reptiles are well studied, the genetic mechanisms that underlie these changes are not known. We used the viviparous African Ocellated Skink, Chalcides ocellatus, as a model to identify a near complete gene expression profile associated with pregnancy using RNA-Seq analyses of uterine transcriptomes. Pregnancy in C. ocellatus is associated with upregulation of uterine genes involved with metabolism, cell proliferation and death, and cellular transport. Moreover, there are clear parallels between the genetic processes associated with pregnancy in mammals and Chalcides in expression of genes related to tissue remodeling, angiogenesis, immune system regulation, and nutrient provisioning to the embryo. In particular, the pregnant uterine transcriptome is dominated by expression of proteolytic enzymes that we speculate are involved both with remodeling the chorioallantoic placenta and histotrophy in the omphaloplacenta. Elements of the maternal innate immune system are downregulated in the pregnant uterus, indicating a potential mechanism to avoid rejection of the embryo. We found a downregulation of major histocompatability complex loci and estrogen and progesterone receptors in the pregnant uterus. This pattern is similar to mammals but cannot be explained by the mammalian model. The latter finding provides evidence that pregnancy is controlled by different endocrinological mechanisms in mammals and reptiles. Finally, 88% of the identified genes are expressed in both the pregnant and the nonpregnant uterus, and thus, morphological and physiological changes associated with C. ocellatus pregnancy are likely a result of regulation of genes continually expressed in the uterus rather than the initiation of expression of unique genes.
As the basis for comparative biology, correctly assigning character homology is critical. Yet, identifying homologous characters in practice is often challenging. Among the major roadblocks is that the mechanistic bases of character homology remain in question. Thus, investigators must rely on several independent lines of evidence (e.g., character anatomy, phylogenetic distribution, or embryological position); however, these distinct sources of evidence often lead to conflicting diagnoses of character homology. What is more, there is no consensus regarding the relative importance of distinct lines of evidence for determining character homology. Here, we review the difficulties that have hindered the search for the mechanistic bases of character identity, and relate these issues to a recently proposed mechanistic hypothesis of character identity--the Character Identity Network Hypothesis. Next, using two well-studied cases of homology conflict (i.e., avian and skink digit identity), we assess the utility of different lines of evidence in diagnosing homology. We conclude that, when comparing adult structures, because anatomical characters more closely reflect the actions of the developmental genetic mechanisms of character individuation they are more reliable than embryological homology criteria.
Morphological characters are the result of developmental gene expression. The identity of a character is ultimately grounded in the gene regulatory network directing development and thus whole-genome gene expression data can provide evidence about character identity. This approach has been successfully used to assess cell-type identity1, 2, 3. Here we use transcriptomic data to address a long-standing uncertainty in evolutionary biology, the identity of avian wing digits4, 5. Embryological evidence clearly identifies the three wing digits as developing from digit positions 2, 3 and 4 (ref. 6), whereas palaeontological data suggest that they are digits I, II and III7. We compare the transcriptomes of the wing and foot digits and find a strong signal that unites the first wing digit with the first foot digit, even though the first wing digit develops from embryological position 2. Interestingly, our transcriptomic data of the posterior digits show a higher degree of differentiation among forelimb digits compared with hindlimb digits. These data show that in the stem lineage of birds the first digit underwent a translocation from digit position 1 to position 2, and further indicate that the posterior wing digits have unique identities contrary to any model of avian digit identity proposed so far5, 8.
Developmental plasticity is thought to reconcile the constraining role of natural selection in maintaining local adaptation with evolutionary diversification under novel conditions, but empirical documentations are rare. In vertebrates, growth and development of bones is partially guided by contractions of attached musculature and such muscle activity changes progressively through embryonic development from sporadic motility to direct functional effects. In species with short generation times, delayed skull maturation extends the guiding effects of muscle activity on formation of foraging morphology into adulthood, providing an opportunity to directly examine the links between plasticity of bone development, ecological adaptations, and evolutionary diversification in foraging morphology. In this case, the morphological consequences of inputs due to local functional requirements should be evident in adaptive divergence across taxa. Here we provide evidence that epigenetic regulation of bone growth in Soricid shrews may enable both development of local adaptations and evolutionary divergence in mandibular morphology. We contrast the effects of muscle stimulation on early- vs. late-maturing components of, foraging apparatus to show that the morphology of late-maturing components is more affected by functional requirements than are early-ossifying traits. Further, the divergence in foraging morphology across shrew species occurs along the directions delineated by inductive effects of muscle loading and bite force on bone formation in late-maturing but not early-maturing mandible components within species. These results support the hypothesis that developmental plasticity can link maintenance of local adaptations with evolutionary diversification in morphology.
1. Ecological convergence in morphology among taxa of distinct evolutionary histories is a common illustration of the efficacy of natural selection. Ecological convergence is often enabled by functional redundancy of complex morphological structures, such that modification of existing morphologies in response to similar functional requirements can lead to the development and evolution of morphological diversity. Thus, studies of the mechanisms that enable the development of similar adaptations in taxa with distinct morphologies provide important insights into both the evolution of past adaptations and patterns of future evolutionary divergence.
2. Here, we examine mechanisms that have enabled ecological convergence in foraging morphology among four geographically isolated and morphologically distinct populations of shrews: south-eastern Arizona and north-central New Mexico populations of the montane shrews (Sorex monticolus) and northern California and north-central Montana populations of the vagrant shrew (S. vagrans).
3. We show that despite overlap in diet, populations had distinct skeletal and muscular morphologies of the mandible. This association between ecological convergence and morphological uniqueness among populations was enabled by versatility of foraging morphologies that generated similar functional outputs.
4. In addition, we found that populations exhibited unique skeletal and muscular correlations with diet suggesting that distinct muscular and morphological components of the complex foraging apparatus can be used for a particular resource. This result corroborates a previous finding that extensive modularity in mandibular development allows diverse morphologies to generate equivalent functions and utilize similar resources across taxa.
5.Synthesis. We conclude that the observed functional and ecological convergences resulted from population-specific musculoskeletal interactions, and suggest that the differences in skeletal and muscular morphologies observed among these populations reflect evolved differences in plasticity of the skeletal and muscular components of the mandible.
Digit identity in the avian wing is a classical example of conflicting anatomical and embryological evidence regarding digit homology. Anatomical in conjunction with phylogenetic evidence supports the hypothesis that the three remaining digits in the bird wing are digits 1, 2, and 3. At the same time, various lines of embryological evidence support the notion that these digits develop in positions that normally produce digits 2, 3, and 4. In recent years, gene expression as well as experimental evidence was published that supports the hypothesis that this discrepancy arose from a digit identity shift in the evolution of the bird wing. A similar but less well-known controversy has been ongoing since the late 19th century regarding the identity of the digits of the three-toed Italian skink, Chalcides chalcides. Comparative anatomy identifies these digits as 1, 2, and 3, while embryological evidence suggests their derivation from embryological positions 2, 3, and 4. Here we re-examine this evidence and add gene expression data to determine the identity of the three digits of C. chalcides. The data confirm that the adult and the embryological evidence for digit identity are in conflict, and the expression of Hoxd11 suggests that digits 1, 2, and 3 develop in positions 2, 3, and 4. We conclude that in C. chalcides, and likely in its close relatives, a digit identity frame shift has occurred, similar to the one in avian evolution. This result suggests that changes in of digit identity might be a more frequent consequence of digit reduction than previously assumed.
The evolutionary importance of maternal effects is determined by the interplay of maternal adaptations and strategies, offspring susceptibility to these strategies, and the similarity of selection pressures between the two generations. Interaction among these components, especially in species where males and females differ in the costs and requirements of growth, limits inference about the evolution of maternal strategies from their expression in the offspring phenotype alone. As an alternative approach, we examine divergence in the proximate mechanisms underlying maternal effects across three house finch populations with contrasting patterns of sex allocation: an ancestral population that shows no sex-biased ovulation, and two recently established populations at the northern and southern boundaries of the species range that have opposite sequences of ovulation of male and female eggs. For each population, we examined how oocyte acquisition of hormones, carotenoids and vitamins was affected by oocyte growth and overlap with the same and opposite sexes. Our results suggest that sex-specific acquisition of maternal resources and sex determination of oocytes are linked in this system. We report that acquisition of testosterone by oocytes that become males was not related to growth duration, but instead covaried with temporal exposure to steroids and overlap with other male oocytes. In female oocytes, testosterone acquisition increased with the duration of growth and overlap with male oocytes, but decreased with overlap with female oocytes. By contrast, acquisition of carotenoids and vitamins was mostly determined by organism-wide partitioning among oocytes and oocyte-specific patterns of testosterone accumulation, and these effects did not differ between the sexes. These results provide important insights into three unresolved phenomena in the evolution of maternal effects - (i) the evolution of sex-specific maternal allocation in species with simultaneously developing neonates of both sexes; (ii) the link between sex determination and sex-specific acquisition of maternal products; and (iii) the evolution of context-dependent modulation of maternal effects.
Divergent selection on traits involved in both local adaptation and the production of mating signals can strongly facilitate population differentiation. Because of its links to foraging morphologies and cultural inheritance song of birds can contribute particularly strongly to maintenance of local adaptations. In two adjacent habitats2014native Sonoran desert and urban areas2014house finches (Carpodacus mexicanus) forage on seeds that are highly distinct in size and shell hardness and require different bite forces and bill morphologies. Here, we first document strong and habitat-specific natural selection on bill traits linked to bite force and find adaptive modifications of bite force and bill morphology and associated divergence in courtship song between the two habitats. Second, we investigate the developmental basis of this divergence and find that early ontogenetic tissue transformation in bill, but not skeletal traits, is accelerated in the urban population and that the mandibular primordia of the large-beaked urban finches express bone morphogenetic proteins (BMP) earlier and at higher level than those of the desert finches. Further, we show that despite being geographically adjacent, urban and desert populations are nevertheless genetically distinct corroborating findings of early developmental divergence between them. Taken together, these results suggest that divergent selection on function and development of traits involved in production of mating signals, in combination with localized learning of such signals, can be very effective at maintaining local adaptations, even at small spatial scales and in highly mobile animals.
Evolutionary diversifications are commonly attributed to the continued modifications of a conserved genetic toolkit of developmental pathways, such that complexity and convergence in organismal forms are assumed to be due to similarity in genetic mechanisms or environmental conditions. This approach, however, confounds the causes of organismal development with the causes of organismal differences and, as such, has only limited utility for addressing the cause of evolutionary change. Molecular mechanisms that are closely involved in both developmental response to environmental signals and major evolutionary innovations and diversifications are uniquely suited to bridge this gap by connecting explicitly the causes of within-generation variation with the causes of divergence of taxa. Developmental pathways of bone formation and a common role for bone morphogenetic proteins (BMPs) in both epigenetic bone remodeling and the evolution of major adaptive diversifications provide such opportunity. We show that variation in timing of ossification can result in similar phenotypic patterns through epigenetically induced changes in gene expression and propose that both genetic accommodation of environmentally induced developmental pathways and flexibility in development across environments evolve through heterochronic shifts in bone maturation relative to exposure to unpredictable environments. We suggest that such heterochronic shifts in ossification can not only buffer development under fluctuating environments while maintaining epigenetic sensitivity critical for normal skeletal formation, but also enable epigenetically induced gene expression to generate specialized morphological adaptations. We review studies of environmental sensitivity of BMP pathways and their regulation of formation, remodeling, and repair of cartilage and bone to examine the hypothesis that BMP-mediated skeletal adaptations are facilitated by evolved reactivity of BMPs to external signals. Surprisingly, no empirical study to date has identified the molecular mechanism behind developmental plasticity in skeletal traits. We outline a conceptual framework for future studies that focus on mediation of phenotypic plasticity in skeletal development by the patterns of BMP expression.
Diversity in organismal forms among taxa is thought to reflect distinct selection pressures across environments. The central assumption underlying this expectation is that taxa experiencing similar selection have similar response to that selection. However, because selection acts on trait function, taxa similarity in selection response depends crucially on the relationship between function and morphology. Further, when a trait consists of multiple parts, changes in function in response to selection can result from modification of different parts, and adaptation to the same environment might result in functional but not morphological similarity. Here, we address the extent to which functional and morphological diversity in masticatory apparatus of soricid shrews reflects a shared ecological characteristic of their diet type. We examine the factors limiting morphological variation across shrew species by assessing the relative contribution of trait function (biomechanics of the jaw), ecology, and phylogeny to species similarity in mandibular traits. We found that species that shared diet type were functionally but not morphologically similar. The presence of multiple semi-independently varying traits enabled functional equivalence of composite foraging morphologies and resulted in variable response to selection exerted by similar diet. We show that functional equivalence of multiple morphologies enabled persistence of differences in habitat use (e.g., habitat moisture and coverage) among species that specialize on the same diet. We discuss the importance of developmental and functional integration among traits for evolutionary diversification of morphological structures that generate equivalent functions.
Examination of historical persistence of integration patterns provides an important insight into understanding the origin and evolution of complex traits. Specifically, the distinct effects of developmental and functional integration on the evolution of complex traits are often overlooked. Because patterns of functional integration are commonly shaped by selection exerted by the external environment, whereas patterns of developmental integration can be determined by relatively environment-independent selection for developmental homeostasis, examination of historical persistence of morphological integration patterns among species should reveal the relative importance of current selection in the evolution of complex traits. We compared historical persistence of integration patterns produced by current developmental versus ecological requirements by examining the evolution of complex mandibular structures in nine species of soricid shrews. We found that, irrespective of phylogenetic relatedness of species, patterns of developmental and functional integration were highly concordant, suggesting that strong selection for developmental homeostasis favors concordant channeling of both internal and external variation. Overall, our results suggest that divergence in mandible shape among species closely follows variation in functional demands and ecological requirements regardless of phylogenetic relatedness among species.
Maternal modification of offspring sex in birds has strong fitness consequences, however the mechanisms by which female birds can bias sex of their progeny in close concordance with the environment of breeding are not known. In recently established populations of house finches (Carpodacus mexicanus), breeding females lay a sex-biased sequence of eggs when ambient temperature causes early onset of incubation. We studied the mechanisms behind close association of incubation and sex-determination strategies in this species and discovered that pre-ovulation oocytes that produce males and females differed strongly in the temporal patterns of proliferation and growth. In turn, sex-specific exposure of oocytes to maternal secretion of prolactin and androgens produced distinct accumulation of maternal steroids in oocyte yolks in relation to oocyte proliferation order. These findings suggest that sex difference in oocyte growth and egg-laying sequence is an adaptive outcome of hormonal constraints imposed by the overlap of early incubation and oogenesis in this population, and that the close integration of maternal incubation, oocytes' sex-determination and growth might be under control of the same hormonal mechanism. We further document that population establishment and the evolution of these maternal strategies is facilitated by their strong effects on female and offspring fitness in a recently established part of the species range.
Extreme environmental change during growth often results in an increase in developmental abnormalities in the morphology of an organism. The evolutionary significance of such stressinduced variation depends on the recurrence of a stressor and on the degree to which developmental errors can be accommodated by an organism’s ontogeny without significant loss of function. We subjected populations of four species of soricid shrews to an extreme environment during growth and measured changes in the patterns of integration and accommodation of stress-induced developmental errors in a complex of mandibular traits. Adults that grew under an extreme environment had lower integration of morphological variation among mandibular traits and highly elevated fluctuating asymmetry in these traits, compared to individuals that grew under the control conditions. However, traits differed strongly in the magnitude of response to a stressor—traits within attachments of the same muscle (functionally integrated traits) had lower response and changed their integration less than other traits. Cohesiveness in functionally integrated complexes of traits under stress was maintained by close covariation of their developmental variation. Such developmental accommodation of stress-induced variation might enable the individual’s functioning and persistence under extreme environmental conditions and thus provides a link between individual adaptation to stress and the evolution of stress resistance.
Sexual ornaments often consist of several components produced by distinct developmental processes. The complexity of sexual ornaments might be favoured by mate choice of individual components in different environments which ultimately results in weak interrelationships (integration) among the developmental processes that produce these components. At the same time, sexual selection for greater exaggeration of individual components favours their stronger co-dependence on organismal resources. This should ultimately produce stronger condition-mediated integration among ornaments' components in individuals with the most exaggerated ornamentation. Here we distinguish between these two sources of integration by examining the relationship between integration and elaboration of sexual ornamentation in three bird species: two with carotenoid-based sexual ornamentation (the house finch, Carpodacus mexicanus and common redpoll, Carduelis flammea) and a species with melanin-based sexual ornamentation (house sparrow, Passer domesticus). We found that integration of components varied with elaboration of carotenoid-based ornamentation but not of melanin ornamentation. In the house finches, integration was the highest in individuals with small ornaments and decreased with ornament elaboration whereas the pattern was the opposite in common redpolls. These results suggest that in these species integration and complexity of carotenoid-based ornamental components are due to shared condition-dependence of distinct developmental pathways, whereas integration and complexity of the melanin ornamentation is due to organismal integration of developmental pathways and is largely condition- and environment-invariant. Thus, functionally, ornamentation of the house sparrows can be considered a single trait, whereas complexity of the house finch and redpoll ornamentation varies with ornament elaboration and individual condition.
Females in species that produce broods of multiple offspring need to partition resources among simultaneously growing ova, embryos or neonates. In birds, the duration of growth of a single egg exceeds the ovulation interval, and when maternal resources are limited, a temporal overlap among several developing follicles in the ovary might result in a trade-off of resources among them. We studied growth of oocytes in relation to their future ovulation order, sex, and overlap with other oocytes in a population of house finches (Carpodacus mexicanus) where strongly sex-biased maternal effects are favoured by natural selection. We found pronounced differences in growth patterns between oocytes that produced males and females. Male oocytes grew up to five times faster and reached their ovulation size earlier than female oocytes. Early onset and early termination of male oocytes' growth in relation to their ovulation resulted in their lesser temporal overlap with other growing ova compared with female oocytes. Consequently, ovulation mass of female but not male oocytes was strongly negatively affected by temporal overlap with other oocytes. In turn, mass of male oocytes was mostly affected by the order of ovulation and by maternal incubation strategy. These results provide a mechanism for sex-biased allocation of maternal resources during egg formation and provide insights into the timing of the sex-determining meiotic division in relation to ovulation in this species.