Intraspecific Variation in Developmental Characters: The Origin of Evolutionary Novelties

Evolutionary developmental biology is inevitably a comparativesubject. However, the taxonomic level at which comparisons canbe made varies widely, and this greatly affects the kind ofinformation that can be gained from the comparison. Broadlyspeaking, high-level comparisons (e.g., between phyla) are moreinformative about phylogenetic pattern and homology, while low-levelcomparisons (e.g., between congeneric species) are more informativeabout evolutionary mechanisms, including speciation. However,so far evolutionary developmental biology has had a relativelyminor input into the traditional territory of population genetics,namely comparisons within species—both within and betweengeographic populations. Yet this area is crucial, as all evolutionarynovelties ultimately arise from intraspecific variation. Here,I address this issue, focusing on the question of how earlyin development novelties arise. To shed light on this question,I discuss two examples of developmental polymorphism withinspecies involving two of the main body axes: anteroposteriorsegmentation in centipedes and left–right asymmetry (chirality)in gastropods.     

Cryptic genetic divergence and associated morphological differentiation in the arboreal land snail Satsuma (Luchuhadra) largillierti (Camaenidae) endemic to the Ryukyu Archipelago, Japan

Land snails are renowned model organisms in evolutionary ecology, but extensive morphological variation and lack of readily available diagnostic characters often invite taxonomic confusion among closely related species. Satsuma (Luchuhadra) largillierti is an arboreal land snail endemic to Okinawa Island, Japan, in which extensive geographic variation in shell morphology has long caused taxonomic complication. To establish robust species limits among S. largillierti and its allies, we perform molecular and morphological analyses of snails sampled from the entire range of Luchuhadra. Analyses of the mitochondrial cytochrome oxidase subunit 1 gene and nuclear ribosomal internal transcribed spacer sequences divide S. largillierti into two, reproductively isolated groups. Each of these groups includes Satsuma erabuensis and Satsuma sooi, respectively, which occur on a nearby island and were traditionally regarded as distinct species. Morphometric analysis of the genitalia further provides clear difference between the two groups, whereas differentiation in shell morphology is slight if any. These results indicate that the traditional taxonomy has overly depended on inadequate morphological difference and a priori information of island geography, which resulted in oversimplification of complex speciation history in Luchuhadra.     

The jewel wasp Nasonia: querying the genome with haplo-diploid genetics

The jewel wasp Nasonia vitripennis is considered the "Drosophila melanogaster of the Hymenoptera." This diminutive wasp offers insect geneticists a means for applying haplo-diploid genetics to the analysis of developmental processes. As in bees, haploid males develop from unfertilized eggs, while diploid females develop from fertilized eggs. Nasonia's advantageous combination of haplo-diploid genetics and ease of handling in the laboratory facilitates screening the entire genome for recessive mutations affecting a developmental process of interest. This approach is currently directed toward understanding the evolution of embryonic pattern formation by comparing Nasonia embryogenesis to that of Drosophila. Haplo-diploid genetics also facilitates developing molecular maps and mapping polygenic traits. Moreover, Nasonia embryos are also proving amenable to cell biological analysis. These capabilities are being exploited to understand a variety of behavioral, developmental, and evolutionary processes, ranging from cytoplasmic incompatibility to the evolution of wing morphology.     

Fishing for genes influencing vertebrate behavior: zebrafish making headway

The zebrafish (Danio rerio) has been a favorite model of developmental biologists and geneticists, but only recently have investigators begun to appreciate its usefulness in behavior genetics. Papers focusing on the behavior or brain function of this species were once extremely rare, but during the past decade rapid growth has taken place. Despite the increased interest, however, the number of studies devoted to the analysis of the behavior of this species is still orders of magnitude less than those conducted on more traditional laboratory subjects including the rat and the mouse. The authors review selected literature and demonstrate that zebrafish is an excellent subject for behavior genetics research, especially in the area of forward genetics (mutagenesis).     

Zebrafish as the Best Vertebrate Model for Development Studies

从八十年代初开始的、通过突变体分离早期胚胎发育基因的研究,揭示了无脊椎动物果蝇形态发生的分子机制,成为１９９５年诺贝尔生理或医学奖的主要内容,同时也标志着发育生物学已经成为生物学的带头学科。该成果的取得得益于果蝇具备发育生物学研究模型的特点,即可同时进行胚胎学和发育遗传学研究。在脊椎动物发育生物学研究方面,由于缺少适当的研究模型,有关早期胚胎发育基因表达调控的研究始终未获突破性进展。包括小鼠、鸡、爪蟾等在内的一些脊椎动物都只适用于胚胎学或者遗传学某一学科的研究,均不是理想的发育生物学研究模型。一种小型的鲤科鱼———斑马鱼,逐渐成为发育生物学研究的最佳脊椎动物模型。它光周期产卵,卵大,胚胎在体外发育,胚胎发育速度快,早期胚胎完全透明,这些特点使它成为很好的脊椎动物胚胎学研究模型;同时,它个体小,产卵量大,产卵周期短,单倍体、雌核发育二倍体的制作和突变体的获得均较容易,精子可以冷冻保存,所有这些特点又使斑马鱼非常适合于发育遗传学研究。本文将详细论述斑马鱼作为脊椎动物发育生物学研究模型的特点,以及作为模型动物正在进行的有关工作。     

Embryology and evolution 1920-1960: worlds apart?

During the early part of the 20th century most embryologists were skeptical about the significance of Mendelian genetics to embryological development. A few embryologists began to study the developmental effects of Mendelian genes around 1940. Such work was a necessary step on the path to modern developmental biology. It occurred during the time when the Evolutionary Synthesis was integrating Mendelian and population genetics into a unified evolutionary theory. Why did the first embryological geneticists begin their study at that particular time? One possible explanation is that developmental genetics was a potential avenue of alliance between embryology and evolutionary biology, two fields that had been separated since the 1890s. To assess this possible motive it is necessary to explore the methodological contrasts that obtained between embryology and both Mendelian-chromosomal genetics and neo-Darwinian evolutionary theory. Some of these contrasts persist to the present day.     

Selfish Genes and Plant Speciation

A key to understand the process of speciation is to uncover the genetic basis of hybrid incompatibilities. Selfish genetic elements (SGEs), DNA sequences that can spread in a population despite being associated with a fitness cost to the individual organism, make up the largest component in many plant genomes, but their role in the genetics of speciation has long been controversial. However, the realization that many organisms have evolved a variety of suppressor mechanisms that reduce the deleterious effects of SGEs has spurred renewed interest in their importance for speciation. The relationship between SGEs and their suppressors often results in strong selection on at least two interacting loci and this arms race therefore creates a situation where SGEs may give rise to hybrid dysgenesis due to Bateson–Dobzhansky–Muller incompatibilities (BDMIs). Here, I argue that examples of SGEs underlying BDMIs may be particularly common among plants compared to other taxa and that a focus on loci involved in genetic conflicts may be especially useful for workers interested in the genetics of plant speciation. I first discuss why the frequent mating system shifts and hybridization events in plants make for a specifically dynamic relationship between SGEs and plant host genomes. I then review some recent empirical observations consistent with SGE-induced speciation in plants. Lastly, I suggest some future directions to test fully the utility of this perspective.     

PERSPECTIVE: FROM MUTANTS TO MECHANISMS? ASSESSING THE CANDIDATE GENE PARADIGM IN EVOLUTIONARY BIOLOGY

The generation of mutants in model organisms by geneticists and developmental biologists over the last century has occasionally produced phenotypes that are startlingly reminiscent of those seen in other species. Such extreme mutations have generally been dismissed by evolutionary geneticists since the "modern synthesis" as irrelevant to adaptation and speciation. But only in recent years has information on the molecular bases of mutant phenotypes become widely available, and thus work on testing the relevance of such extreme mutations to the generation of phylogenetic diversity has just begun. Here we evaluate whether evolutionary mimics are, in fact, useful for pinpointing the genetic differences that distinguish morphological variants generated during evolution. Examples come from both plants and animals, and range from intraspecific to interordinal taxonomic ranges. The use of mutationally defined candidate genes to predict evolutionary mechanisms has so far been most fruitful in explaining intraspecific variants, where it has been effective in both plants and animals. In several cases these efforts were facilitated or supported by parallel results from quantitative trait loci studies, in which natural alleles controlling continuous variation in developmental model organisms were mapped to mutationally defined genes. However, despite these successes the approach's utility seems to rapidly decay as a function of phylogenetic distance. This suggests that the divergence of developmental genetic systems is great even in closely related organisms and may become intractable at larger distances. We discuss this result in the context of what it teaches us about development, the future prospects of the candidate gene approach, and the historical debate over process in micro- and macroevolution.     

Slow genital and genetic but rapid non-genital and ecological differentiation in a pair of spider species (Araneae,Pholcidae)

Like most animals with internal fertilization, spiders tend to have species-specific genitalia, allowing closely related species to be identified by their reproductive morphology more easily than by non-genital characters. This implies that genitalia evolve on average more rapidly than non-genital morphological traits. Here we describe two putative species of Pholcidae from Taiwan (Pholcus pingtung, n. sp.; Pholcus chengpoi, n. sp.) that differ conspicuously in their microhabitat (rocks vs. leaves), coloration, color pattern, and body proportions, but have almost indistinguishable genitalia and cytochrome oxidase I (co1) sequences. The two species have identical yet highly unusual male cheliceral modifications, strongly arguing for sister species. Despite the almost identical genitalia and co1 sequences, we treat the two ‘morphs’ as species for three reasons: (1) they are easily distinguished by several characters; no intermediate specimens were found; (2) subtle yet consistent differences in genital (uncus) shape support the idea of reproductively isolated entities beyond the more conspicuous non-genital differences; (3) each locality provided both types of microhabitat but only one of the two species, arguing against environmental plasticity or polymorphism. We conclude that probably a very recent expansion into a novel microhabitat has led to speciation and rapid ecological and non-genital differentiation, with insufficient time to accumulate significant genital and genetic differences.     

Medical and human genetics 1977: trends and directions

Our field is in a rapid state of evolution. The broader concerns of human genetics not of immediate medical interest such as behavioral genetics are often investigated by persons not trained or identified as human geneticists. Both medical genetics and human genetics in general have prospered when various biologic techniques have been applied to genetic concepts. A search for novel biologic methods may provide new insights and may bridge the gulf between Mendelian and biometric approaches in studies of behavior and of common diseases. Medical geneticists need to broaden their fields of interest to encompass other fields than those of pediatric interest alone. We need to attract more basic scientists. Our field is evolving from a largely research oriented science to a service-oriented specialty. This logical development is a sign of increasing maturity and makes available to the public the results of our research. The resulting stresses and strains need careful watching to prevent their slowing the momentum of our science which can contribute continued insights into the many problems of behavior, health, and disease.     

Geometric morphometrics reveal male genitalia differences in the Lasiommata megera/paramegaera complex (Lepidoptera, Nymphalidae) and the lack of a predicted hybridization area in the Tuscan Archipelago

The recognition of specific demarcation between allopatric populations, as for island endemics, is particularly difficult according to the Biological Concept of Species. However, the recognition of the specific status of island taxa is decisive in evaluating important areas of endemism for conservation purposes. The recent taxonomic inflation of European butterfly species calls into question the validity and objectivity of taxonomic practices, and of databases dependent on them, which are used in biogeography and conservation. In this paper I applied rigorous morphometric analyses instead of visual evaluation to solve the long debated question of whether Lasiommata paramegaera butterfly from Sardinia and Corsica should be considered as a separated entity from the widespread Lasiommata megera . First, I carried out analyses of male genitalia shape comparing the populations from Corsica and Tuscany. Thereafter, I also searched for possible hybridization evidence in the sole area where it is strongly predicted: the Tuscan Archipelago. These islands are located between Tuscany and Corsica and there is large evidence of a continuous immigration of butterflies from these two main sources. I found that Corsican L. paramegaera and Tuscan L. megera can be clearly distinguished on the basis of genitalia shape. Furthermore, the Lasiommata population of each islet clearly maintains the characteristics of one of the two species without evidence of intermediate individuals. In conclusion, I suggest that the two entities should be considered as separate species maintaining their homogeneity by a reduced gene flow across sea, mating avoidance and/or by some depletion of F1 hybrids in developmental or mating success.     

GENOME DIVERGENCE AND THE GENETIC ARCHITECTURE OF BARRIERS TO GENE FLOW BETWEEN LYCAEIDES IDAS AND L. MELISSA

Genome divergence during speciation is a dynamic process that is affected by various factors, including the genetic architecture of barriers to gene flow. Herein we quantitatively describe aspects of the genetic architecture of two sets of traits, male genitalic morphology and oviposition preference, that putatively function as barriers to gene flow between the butterfly species Lycaeides idas and L. melissa. Our analyses are based on unmapped DNA sequence data and a recently developed Bayesian regression approach that includes variable selection and explicit parameters for the genetic architecture of traits. A modest number of nucleotide polymorphisms explained a small to large proportion of the variation in each trait, and average genetic variant effects were nonnegligible. Several genetic regions were associated with variation in multiple traits or with trait variation within‐ and among‐populations. In some instances, genetic regions associated with trait variation also exhibited exceptional genetic differentiation between species or exceptional introgression in hybrids. These results are consistent with the hypothesis that divergent selection on male genitalia has contributed to heterogeneous genetic differentiation, and that both sets of traits affect fitness in hybrids. Although these results are encouraging, we highlight several difficulties related to understanding the genetics of speciation.     

Developmental stability and adaptive variability of male genitalia in sexually dimorphic beetles

Animal genitalia often show distinct developmental and evolutionary relationships with other parts of the body. Morphological observations of 29 sexually dimorphic and monomorphic beetle species in 16 genera of families Scarabaeidae and Lucanidae, Coleoptera, in 53 locations revealed that male genitalia size was consistently and distinctly less variable than that of other body parts within the same population, while it differentiated more readily among different populations than other body parts. The most noticeable genitalia size differentiation occurred in populations that coexisted with morphologically and ecologically similar congeneric species. Such differentiation may indicate selection for reproductive isolation. These characteristics of genitalia morphology may have been instrumental in generating the speciation pattern seen in most beetles.     

How theories became knowledge: Morgan's chromosome theory of heredity in America and Britain

T. H. Morgan, A. H. Sturtevant, H. J. Muller and C. B. Bridges published their comprehensive treatise The Mechanism of Mendelian Heredity in 1915. By 1920 Morgan's ``Chromosome Theory of Heredity' was generally accepted by geneticists in the United States, and by British geneticists by 1925. By 1930 it had been incorporated into most general biology, botany, and zoology textbooks as established knowledge. In this paper, I examine the reasons why it was accepted as part of a series of comparative studies of theory-acceptance in the sciences. In this context it is of interest to look at the persuasiveness of confirmed novel predictions, a factor often regarded by philosophers of science as the most important way to justify a theory. Here it turns out to play a role in the decision of some geneticists to accept the theory, but is generally less important than the CTH's ability to explain Mendelian inheritance, sex-linked inheritance, non-disjunction, and the connection between linkage groups and the number of chromosome pairs; in other words, to establish a firm connection between genetics and cytology. It is remarkable that geneticists were willing to accept the CTH as applicable to all organisms at a time when it had been confirmed only for Drosophila. The construction of maps showing the location on the chromosomes of genes for specific characters was especially convincing for non-geneticists.     

Natural selection and genital variation: a role for the environment,parasites and sperm ageing?

Male genitalia are more variable between species (and populations) than other organs, and are more morphologically complex in polygamous compared to monogamous species. Therefore, sexual selection has been put forward as the major explanation of genital variation and complexity, in particular cryptic female choice for male copulatory courtship. As cryptic female choice is based on differences between males it is somewhat paradoxical that there is such low within-species variation in male genitalia that they are a prime morphological identification character for animal species. Processes other than sexual selection may also lead to genitalia variation but they have recently become neglected. Here I focus on pleiotropy and natural selection and provide examples how they link genitalia morphology with genital environments. Pleiotropy appears to be important because most studies that specifically tested for pleiotropic effects on genital morphology found them. Natural selection likely favours certain genital morphology over others in various environments, as well as by reducing re-infection with sexually transmitted diseases or reducing the likelihood of fertilisation with aged sperm. Both pleiotropy and natural selection differ locally and between species so may contribute to local variation in genitalia and sometimes variation between monogamous and polygamous species. Furthermore, the multitude of genital environments will lead to a multitude of genital functions via natural selection and pleiotropy, and may also contribute to explaining the complexity of genitalia.     

Heterochrony and growth rate variation mediate the development of divergent genital morphologies in closely related Ohomopterus ground beetles

The rapid divergence of genital morphology is well studied in the context of sexual selection and speciation; however, little is known about the developmental mechanisms underlying divergence in genitalia. Ground beetles in the subgenus Ohomopterus genus Carabus have species‐specific genitalia that show coevolutionary divergence between the sexes. In this study, using X‐ray microcomputed tomography, we examined the morphogenesis of male and female genitalia in two closely related Ohomopterus species with divergent genital morphologies. The morphogenetic processes generating the male and female genitalia at the pupal stage were qualitatively similar in the two species. The male aedeagus and internal sac and female bursa copulatrix were partially formed at pupation and developed gradually thereafter. The species‐specific genital parts, male copulatory piece, and female vaginal appendix differed in the timing and rate of development. The relatively long copulatory piece of Carabus maiyasanus began to develop earlier, but subsequent rates of growth were similar in the two species. The timing of the formation of the vaginal appendix and initial growth rates were similar, but subsequent rapid growth led to a longer vaginal appendix in C. maiyasanus. Thus, substantial interspecific differences in the size of genital parts were mediated by different underlying developmental mechanisms between the sexes (i.e., a shift in the developmental schedule in males and a change in growth rate in females). These results revealed the spatio–temporal dynamics of species‐specific genital structure development, providing a novel platform for evo–devo studies of the diversification of genital morphologies.     

The interaction of sexually and naturally selected traits in the adaptive radiations of cichlid fishes

The question of how genetic variation translates into organismal diversity has puzzled biologists for decades. Despite recent advances in evolutionary and developmental genetics, the mechanisms that underlie adaptation, diversification and evolutionary innovation remain largely unknown. The exceptionally diverse species flocks of cichlid fishes are textbook examples of adaptive radiation and explosive speciation and emerge as powerful model systems to study the genetic basis of animal diversification. East Africa's hundreds of endemic cichlid species are akin to a natural mutagenesis screen and differ greatly not only in ecologically relevant (hence naturally selected) characters such as mouth morphology and body shape, but also in sexually selected traits such as coloration. One of the most fascinating aspects of cichlid evolution is the frequent occurrence of evolutionary parallelisms, which has led to the question whether selection alone is sufficient to produce these parallel morphologies, or whether a developmental or genetic bias has influenced the direction of diversification. Here, I review fitness-relevant traits that could be responsible for the cichlids' evolutionary success and assess whether these were shaped by sexual or natural selection. I then focus on the interaction and the relative importance of sexual vs. natural selection in cichlid evolution. Finally, I discuss what is currently known about the genes underlying the morphogenesis of adaptively relevant traits and highlight the importance of the forthcoming cichlid genomes in the quest of the genetic basis of diversification in this group.