Inbreeding shapes the evolution of marine invertebrates

Inbreeding is a potent evolutionary force shaping the distribution of genetic variation within and among populations of plants and animals. Yet, our understanding of the forces shaping the expression and evolution of nonrandom mating in general, and inbreeding in particular, remains remarkably incomplete. Most research on plant mating systems focuses on self-fertilization and its consequences for automatic selection, inbreeding depression, purging, and reproductive assurance, whereas studies of animal mating systems have often assumed that inbreeding is rare, and that natural selection favors traits that promote outbreeding. Given that many sessile and sedentary marine invertebrates and marine macroalgae share key life history features with seed plants (e.g., low mobility, modular construction, and the release of gametes into the environment), their mating systems may be similar. Here, we show that published estimates of inbreeding coefficients (F_IS) for sessile and sedentary marine organisms are similar and at least as high as noted in terrestrial seed plants. We also found that variation in F_IS within invertebrates is related to the potential to self-fertilize, disperse, and choose mates. The similarity of F_IS for these organismal groups suggests that inbreeding could play a larger role in the evolution of sessile and sedentary marine organisms than is currently recognized. Specifically, associations between traits of marine invertebrates and F_IS suggest that inbreeding could drive evolutionary transitions between hermaphroditism and separate sexes, direct development and multiphasic life cycles, and external and internal fertilization.     

Correlated evolution of self-incompatibility and clonal reproduction in Solanum (Solanaceae)

It has been suggested that clonality provides reproductive assurance in cross-fertilizing species subject to pollen limitation, relieving one of the main selective pressures favoring the evolution of self-fertilization. According to this hypothesis, cross-fertilizing species subject to pollen limitation should often be clonal. Here, we investigated the association between clonality and a genetic mechanism enforcing outcrossing, self-incompatibility, in Solanum (Solanaceae). We collected self-incompatibility and clonality information on 87 species, and looked for an association between these two traits. To account for the contribution of shared evolutionary history to this association, we incorporated phylogenetic information from chloroplast (NADH dehydrogenase subunit F) sequence data. We found that self-incompatibility is strongly associated with clonal reproduction: all self-incompatible species reproduce clonally, while the absence of clonality is widespread among self-compatible taxa. The observed correlation persists after taking into account shared phylogenetic history, assumptions about the evolutionary history of self-incompatibility, uncertainty associated with phylogeny estimation, and associations with life history (annual/perennial). Our results are consistent with the hypothesis that clonality provides reproductive assurance, and suggest that the consequences of clonal growth in the evolution of plant reproductive strategies may be more significant than previously thought.     

Darwin’s “Mr. Arthrobalanus”: Sexual Differentiation,Evolutionary Destiny and the Expert Eye of the Beholder

Darwin’s Cirripedia project was an exacting exercise in systematics, as well as an encrypted study of evolution in action. Darwin had a long-standing interest and expertise in marine invertebrates and their sexual arrangements. The surprising and revealing sexual differentiation he would uncover amongst barnacles represented an important step in his understanding of the origins of sexual reproduction. But it would prove difficult to reconcile these findings with his later theorizing. Moreover, the road to discovery was hardly straightforward. Darwin was both helped and hindered by the tacit expectations generated by his transformist theorizing, and had to overcome culturally-embedded assumptions about gender and reproductive roles. Significant observational backtracking was required to correct several oversights and misapprehensions, none more so than those relating to the chronically misunderstood “Mr. Arthrobalanus.” With careful attention to chronology, this paper highlights some curious and overlooked aspects of Darwin’s epic project.     

Interactive analysis of phylogeny and character evolution using the computer program MacClade

Computer programs for phylogenetic analysis have been important tools in systematics and evolutionary biology, but most have been designed primarily for the reconstruction of phylogenetic trees and not the interpretation of patterns of character evolution. Described here is the computer program MacClade, designed for interactive analysis of character evolution and phylogeny. For a given tree and a matrix of character data, MacClade displays its reconstruction of character evolution by shading the branches of the tree to indicate ancestral states. Trees can be manipulated for instance by picking up and moving branches. Assumptions underlying the reconstruction of character evolution can be varied extensively. With these manipulations and MacClade's graphical feedback, one can explore the relationships among phylogenetic trees, character data, assumptions and interpretations of character evolution. MacClade has extensive facilities for editing data, displaying various summaries of character evolution in charts and diagrams, and printing.     

Lineage divergence of a freshwater snail clade associated with post-Tethys marine basin development

The complex evolutionary history of the Eurasian gastropod lineage Theodoxus reflects the evolution of marine basins following the breakup of the Tethys Sea. Today, this clade inhabits the lakes, rivers, streams, and estuaries of Europe, southwestern Asia, and North Africa. Here we present the first phylogenetic hypothesis for this clade. Based upon extensive geographic and taxonomic sampling, portions of the mitochondrial genes for cytochrome c oxidase subunit I and 16S rRNA were sequenced and analysed using maximum likelihood and maximum parsimony methods. Results from bootstrap analyses, Bayesian analysis, and sensitivity analyses lend support to six deep phylogenetic subdivisions within Theodoxus. These major clades are geographically associated with the major post-Tethyan marine basins. Estimates of divergence times using a penalized likelihood approach indicate that divergence of these major lineages occurred during the Miocene, simultaneous with the breakup of the Mediterranean and Paratethys Seas. The resulting major subclades later diversified during the Pliocene, primarily within geographic regions associated with the eastern and western Mediterranean Sea, the Pannonian Basin, and the Black Sea, thus producing the extant species assemblages. Finally, these phylogenetic results imply that much of the current taxonomy is flawed, therefore we offer recommendations for revising the classification of Theodoxus species based on phylogenetic systematics.     

A new look at evolution in the Galápagos: evidence from the late Cenozoic marine molluscan fauna

Endemism is not as common in the marine invertebrate fauna of the Galápagos Islands region as in the adjacent terrestrial biota. Marine invertebrates in the Galápagos are largely cosmopolitan species from the Panamic, Indo-Pacific, Californian, or Peruvian faunal provinces. However, an endemic component is also present in the fauna. The observed pattern among marine invertebrate organisms can be accounted for by at least two processes: (1) genetic continuity between mainland and island populations mediated through planktonic larvae; and (2) lower rates of intrinsic evolutionary change. The evolutionary scenario standardly applied to terrestrial organisms in the Galápagos, namely, adaptive radiation and speciation in reproductive isolation from mainland source populations, does not apply to all marine invertebrates. Evidence in support of the alternative scenario for marine invertebrates comes from both published records of species occurring in the islands and recent studies of fossil-bearing deposits on several islands in the archipelago. Two misconceptions–considering the islands and sedimentary deposits to be older than now thought, and equating the rate of evolution of the terrestrial biota with the marine biota–can lead to an incorrect interpretation of evolution in the Galápagos Contrasts between marine invertebrate and terrestrial organisms serve to illustrate some fundamental differences which have important evolutionary implications. Some of these are: endemism; dispersal; taxonomic relationships; island definitions; rates of evolutionary change; and age of fossils. In terms of Darwin's evolutionary scenario, terrestrial organisms represent the paradigm and marine organisms represent the paradox.     

Evaluating evolutionary pressures and phylogenetic signal in earthworms: a case study – the number of typhlosole lamellae in Hormogastridae (Annelida,Oligochaeta)

Rarely have phylogenetic comparative methods been used to study the correlation between phenotypic traits and environmental variables in invertebrates. With the widespread convergence and conservativeness of the morphological characters used in earthworms, these comparative methods could be useful to improve our understanding of their evolution and systematics. One of the most prominent morphological characters in the family Hormogastridae, endemic to Mediterranean areas, is their multilamellar typhlosole, traditionally thought to be an adaptation to soils poor in nutrients. We tested the correlation of body size and soil characteristics with the number of typhlosole lamellae through a phylogenetic generalized least squares (PGLS) analysis. An ultrametric phylogenetic hypothesis was built with a 2580‐bp DNA sequence from 90 populations, used in combination with three morphological and 11 soil variables. The best‐supported model, based on the Akaike information criterion, was obtained by optimizing the parameters lambda (λ), kappa (κ), and delta (δ). The phylogenetic signal was strong for the number of typhlosole lamellae and average body weight, and was lower for soil variables. Increasing body weight appeared to be the main evolutionary pressure behind the increase in the number of typhlosole lamellae, with soil texture and soil richness having a weaker but significant effect. Information on the evolutionary rate of the number of typhlosole lamellae suggested that the early evolution of this character could have strongly shaped its variability, as is found in an adaptive radiation. This work highlights the importance of implementing the phylogenetic comparative method to test evolutionary hypotheses in invertebrate taxa.     

Developmental genetic evidence for a monophyletic origin of the bilaterian brain

The widely held notion of an independent evolutionary origin of invertebrate and vertebrate brains is based on classical phylogenetic, neuroanatomical and embryological data. The interpretation of these data in favour of a polyphyletic origin of animals brains is currently being challenged by three fundamental findings that derive from comparative molecular, genetic and developmental analyses. First, modern molecular systematics indicates that none of the extant animals correspond to evolutionary intermediates between the protostomes and the deuterostomes, thus making it impossible to deduce the morphological organization of the ancestral bilaterian or its brain from living species. Second, recent molecular genetic evidence for the body axis inversion hypothesis now supports the idea that the basic body plan of vertebrates and invertebrates is similar but inverted, suggesting that the ventral nerve chord of protostome invertebrates is homologous to the dorsal nerve cord of deuterostome chordates. Third, a developmental genetic analysis of the molecular control elements involved in early embryonic brain patterning is uncovering the existence of structurally and functionally homologous genes that have comparable and interchangeable functions in key aspects of brain development in invertebrate and vertebrate model systems. All three of these findings are compatible with the hypothesis of a monophyletic origin of the bilaterian brain. Here we review these findings and consider their significance and implications for current thinking on the evolutionary origin of bilaterian brains. We also preview the impact of comparative functional genomic analyses on our understanding of brain evolution.     

CLUTCH SIZE AND EGG SIZE IN FREE-LIVING AND PARASITIC COPEPODS: A COMPARATIVE ANALYSIS

The evolution of reproductive strategies and the trade-off between number and size of eggs were investigated in a comparative analysis of free-living and parasitic copepods. Data from 1038 copepod species were used to obtain family averages for 105 families; the phylogenetic relationships among these families include 94 branching events or 94 independent contrasts on which the analysis was based. Transition from a free-living existence to parasitism on invertebrates resulted in small increases in body size. Transition from parasitism on invertebrates to parasitism on fish was associated with greater increases in body size. After controlling for body size, a switch to fish hosts resulted in an increase in the number of eggs produced and a reduction in egg size. Among all contrasts, there was a negative relationship between changes in relative clutch size and changes in relative egg size, suggesting the existence of a trade-off between egg size and numbers. However, opposite changes in these measures of clutch size and egg size were not quite more frequent than expected by chance, therefore indicating that investments into egg numbers are not necessarily made at the expense of egg size, and vice versa. Latitude affected copepod body size, clutch size, and egg size, whereas the effects of freshwater colonization or size of the fish host were not significant. Comparative analyses at either the genus or species levels within given taxa of copepods parasitic on fish provided limited support for a trade-off between clutch size and egg size, but were hampered by the small number of independent phylogenetic contrasts available. From the family-level comparative analysis, it appears that the evolutionary transition from a free life to parasitism on invertebrates, and the transition from parasitism on invertebrates to parasitism on fish, have led to changes in life-history traits in response to the different selective pressures associated with the different modes of life.     

Marine gregarines: evolutionary prelude to the apicomplexan radiation?

Gregarine apicomplexans inhabit the intestines, coeloms and reproductive vesicles of invertebrates. An emphasis on specific ancestral characteristics in marine gregarines has given the group a reputation of being 'primitive.' Although some lineages have retained characteristics inferred to be ancestral for the group, and perhaps apicomplexans as a whole, most gregarines represent highly derived parasites with novel ultrastructural and behavioral adaptations. Many marine gregarines have become giants among single-celled organisms and have evolved ornate surface structures. A comparison of gregarine morphology, placed in a modern phylogenetic context, helps clarify the earliest stages of apicomplexan evolution, the origin of Cryptosporidium, and specific cases of convergent evolution within the group and beyond.     

Molecular Phylogenetic Positions and Ultrastructure of Marine Gregarines (Apicomplexa) Cuspisella ishikariensis n. gen., n. sp. and Loxomorpha cf. harmothoe from Western Pacific scaleworms (Polynoidae)

Marine gregarines are unicellular parasites of invertebrates commonly found infecting the intestine and coelomic spaces of their hosts. Situated at the base of the apicomplexan tree, marine gregarines offer an opportunity to explore the earliest stages of apicomplexan evolution. Classification of marine gregarines is often based on the morphological traits of the conspicuous feeding stages (trophozoites) in combination with host affiliation and molecular phylogenetic data. Morphological characters of other life stages such as the spore are also used to inform taxonomy when such stages can be found. The reconstruction of gregarine evolutionary history is challenging, due to high levels of intraspecific variation of morphological characters combined with relatively few traits that are taxonomically unambiguous. The current study combined morphological data with a phylogenetic analysis of small subunit rDNA sequences to describe and establish a new genus and species (Cuspisella ishikariensis n. gen., n. sp.) of marine gregarine isolated from the intestine of a polynoid host (Lepidonotus helotypus) collected from Hokkaido, Japan. This new species possesses a set of unusual morphological traits including a spiked attachment apparatus and sits on a long branch on the molecular phylogeny. Furthermore, this study establishes a molecular phylogenetic position for Loxomorpha cf. harmothoe, a previously described marine gregarine, and reveals a new group of gregarines that infect polynoid hosts.     

Evolutionary relationships among food habit, loss of flight, and reproductive traits: life-history evolution in the Silphinae (Coleoptera: Silphidae)

Flightlessness in insects is generally thought to have evolved due to changes in habitat environment or habitat isolation. Loss of flight may have changed reproductive traits in insects, but very few attempts have been made to assess evolutionary relationships between flight and reproductive traits in a group of related species. We elucidated the evolutionary history of flight loss and its relationship to evolution in food habit, relative reproductive investment, and egg size in the Silphinae (Coleoptera: Silphidae). Most flight-capable species in this group feed primarily on vertebrate carcasses, whereas flightless or flight-dimorphic species feed primarily on soil invertebrates. Ancestral state reconstruction based on our newly constructed molecular phylogenetic tree implied that flight muscle degeneration occurred twice in association with food habit changes from necrophagy to predatory, suggesting that flight loss could evolve independently from changes in the environmental circumstances per se. We found that total egg production increased with flight loss. We also found that egg size increased with decreased egg number following food habit changes in the lineage leading to predaceous species, suggesting that selection for larger larvae intensified with the food habit change. This correlated evolution has shaped diverse life-history patterns among extant species of Silphinae.     

Some problems of regressive evolution

The concept of morphophysiological regress as one of the main ways to biological progress, as well as its major factors (the sedentary and parasitic modes of life), are discussed. Some notions of regressive evolution are critically reviewed. Special attention is paid to evolutionary transformations of the nervous system, one of the main integrating factors in the body. All theories of evolutionary progress based on sedentary organisms are demonstrated to be untenable. The entire progressive evolution of Metazoa has been related to mobile life. Since regressive trends are common in the evolution, the phylogenetic tree of Metazoa requires serious revision.     

Circularity,evolution, systematics … and circularity

Many have argued strongly that incorporation of evolutionary theory into systematics is dangerously circular, while others have maintained that such an integrated approach increases the accuracy of phylogenetic inference. Here, it is demonstrated that such blanket statements regarding exclusion or inclusion of evolutionary principles in systematics fail to distinguish between two very different types of principles. ‘Phylogeny-neutral’ evolutionary principles are those inferred without any recourse to specific phylogenetic hypotheses (e.g. via developmental genetics, biomechanics). In contrast, ‘phylogeny-dependent’ principles are those which can only be inferred on the basis of specific phylogenetic hypotheses (e.g. character associations detected via ‘comparative methods’). Inclusion of phylogeny-neutral principles in systematic studies as a priori assumptions can be justified, since these principles have (often strong) external empirical support from other spheres of investigation. However, inclusion of phylogeny-dependent principles in systematic studies is circular, since such principles have no external empirical support but are themselves derived from systematic studies. Advocating inclusion or exclusion of all (or as many as possible) evolutionary principles from phylogenetic analysis is therefore misguided. Rather, phylogeny-neutral principles are independently supported and can be included, while phylogeny-dependent principles are unjustified assumptions and should be excluded to avoid circularity. However, integration of complex phylogeny-neutral principles in systematics can create operational problems, even though there are no methodological reasons against their inclusion.     

Claims and limits of phylogenetic systematics1

Within the methodology of phylogenetic systematics four hierarchic levels are distinguished: the “Central Claim” (to reconstruct phylogeny), methodoloical postulate (to conclude analysis with a purely dichotomous cladogram if ever possible), method (search for sister-group relationships by character analysis), and “Taxonomic Principle” (establishment of a classification reflecting merely the recognized genealoy). Certain limits of applicability and reliability of traditional phylogenetic systematics are specified: genealogy can only be analysed among taxa with perceptible evolutionary novelties; reticulated genealogy is not yet regarded; events other than cladogenetic ones cannot be recognised. Phylogenetic systematics is an independent method which has not been absorbed by any type of “pattern” or “transformed” cladism. Phylogenetic systematics relies on the theory of evolution, which does not lead into circularity, since phylogenetic systematics does not claim to prove or to explain evolution whatsoever.     

Über die Beziehung zwischen Systematik und Evolution

The relation between systematics and evolution The theoretical and methodological decoupling of pattern analysis from the causal explanation of the hierarchical order of nature by the hypothesis of descent with modification is defended. This contrasts with the philosophy of phylogenetic systematics which views acceptance of evolutionary theory as a necessary prerequisite for research in systematics.     

Systematics and evolutionary biology of the fern genusHymenasplenium (Aspleniaceae)

In Aspleniaceae,Hymenasplenium is a well-defined group with dorsiventral creeping rhizomes. Members ofHymenasplenium are widely distributed in the tropic zones of the world and have great variation in morphology and ecolgy, making it a good model group for plant systematics and evolutionary biology. I have worked on this group using techniques such as comparative morphology, ecology, cytology (for examining chromosomes and reproductive modes), phytochemistry and molecular biology. I considered the evolution of various phenetic characters based on a molecular phylogenetic tree which I recently obtained from sequence comparisons ofrbcL. In this paper, I will summarize the results. Recipient of the Botanical Society Award for Young Scientists, 1993.     

Live history evolution in Serpulimorph polychaetes: a phylogenetic analysis

The widely accepted hypothesis of plesiomorphy of planktotrophic, and apomorphy of lecithotrophic, larval development in marine invertebrates has been recently challenged as a result of phylogenetic analyses of various taxa. Here the evolution of planktotrophy and lecithotrophy in Serpulimorph polychaetes (families Serpulidae and Spirorbidae) was studied using a hypothesis of phylogenetic relationships in this group. A phylogenetic (parsimony) analysis of 36 characters (34 morphological, 2 developmental) was performed for 12 selected serpulid and 6 spirorbid species with known reproductive/developmental strategies. Four species of Sabellidae were used in the outgroup. The analysis yielded 4 equally parsimonious trees of 78 steps, with a consistency index (CI) of 0.654 (CI excluding uninformative characters is 0.625). Under the assumption of unweighted parsimony analysis, planktotrophic larvae are apomorphic and non-feeding brooded embryos are plesiomorphic in serpulimorph polychaetes. The estimated polarity of life history transitions may be strengthened by further studies demonstrating an absence of a unidirectional bias in planktotrophy-lecithotrophy transition in polychaetes.     

Diversity-enhancing selection acts on a female reproductive protease family in four subspecies of Drosophila mojavensis

Protein components of the Drosophila male ejaculate are critical modulators of reproductive success, several of which are known to evolve rapidly. Recent evidence of adaptive evolution in female reproductive tract proteins suggests this pattern may reflect sexual selection at the molecular level. Here we explore the evolutionary dynamics of a five-paralog gene family of female reproductive proteases within geographically isolated subspecies of Drosophila mojavensis. Remarkably, four of five paralogs show exceptionally low differentiation between subspecies and unusually structured haplotypes that suggest the retention of old polymorphisms. These gene genealogies are accompanied by deviations from neutrality consistent with diversifying selection. While diversifying selection has been observed among the reproductive molecules of mammals and marine invertebrates, our study provides the first evidence of this selective regime in any Drosophila reproductive protein, male or female.     

WHY ARE THERE SO MANY SPECIES OF BROODING ANTARCTIC ECHINOIDS?

Marine invertebrates display a great variety of life-history traits and reproductive strategies. In echinoids, four patterns of larval development are generally recognized: planktotrophy, pelagic lecithotrophy, bottom dwelling, and brood protecting. Each broad type of free and protected development is found in all the oceans, but comparisons of the principal reproductive modes between different geographic regions have shown that they are not equally distributed. Frequency of pelagic development (planktotrophic and lecithotrophic) decreases from equator to Antarctic, where brood protecting becomes dominant. Numerous theories have been proposed to explain the richness of nonpelagic development in most marine invertebrates within the Southern Ocean. These theories can be grouped into three categories: (1) larval survival, where selection acts on larval; (2) energy allocation; and (3) dispersal. All of them consider the adaptative significance of brood protecting as the key to the success of this strategy in the Antarctic. However, the adaptative significance of brooding and the evolutionary success of this strategy in the Antarctic must be considered as two separate questions. To consider the problem at an evolutionary level, we have examined the consequences of different reproductive strategies on the genetic structure of species and on the long-term evolution of the clade. We examine this problem in the case of echinoids, a clade particularly well suited to addressing this question. In echinoids, the reduction of larval-stage duration is associated with a decrease in gene flow and consequently in the geographical scale of genetic differentiation. This allows us to reconsider the high-speciation-rate model, which leads to an increase in the number of low-dispersal species (isolation by distance). This model, previously tested by means of fossils is not satisfactory in living echinoids. Thus, the model is rebuilt with the addition of differential extinction rate between planktotrophic and brooding species in relation with the climatic history of the Antarctic.