A phylogenetic analysis of variation in reproductive mode within an Australian lizard (Saiphos equalis, Scincidae)

Saiphos equalis , a semi-fossorial scincid lizard from south-eastern Australia, is one of only three reptile species world-wide that are known to display geographic variation in reproductive mode. Uniquely, Saiphos equalis includes populations with three reproductive modes: oviparous with long (15-day) incubation periods; oviparous with short (5-day) incubation periods; and viviparous (0-day incubation periods). No Saiphos populations show 'normal' scincid oviparity (> 30-day incubation period). We used mitochondrial nucleotide sequences ( ND2 and cytochrome b ) to reconstruct relationships among populations from throughout the species' distribution in New South Wales, Australia. Under the phylogenetic species concept, phylogenetic analyses are consistent with the oviparous and viviparous populations of S. equalis being conspecific. Phylogenetic analyses suggest that the long incubation period oviparous lineage is the sister group to all other populations; and that the viviparous populations belong to a cluster of weakly supported clades basal to the short-incubation-period oviparous clade. These clades correspond to variation in reproductive mode and geographic location.     

Humidity levels drive reproductive modes and phylogenetic diversity of amphibians in the Brazilian Atlantic Forest

Aim The diversity of reproductive modes among amphibians constitutes a striking example of how differences in the biology of species provide important explanations for species distribution patterns on a broad scale. We hypothesize that sites with a higher humidity level will support more modes of reproduction than drier sites and will consequently exhibit a higher phylogenetic diversity. Furthermore, if there is a gradient in the tolerance of reproductive modes to desiccation, there will be a nested pattern in the composition of reproductive modes among sites. Location Twenty‐seven forest sites in the Brazilian Atlantic Forest. Methods Through a path analysis approach, we evaluated the direct and indirect effects of the humidity level on the number of reproductive modes, as well as the relative importance of both variables on amphibian phylogenetic diversity. A nestedness analysis was used to quantify the extent to which the compositions of both species and reproductive modes in drier sites correspond to subsets of those in sites with higher annual precipitation. Results We found that the reproductive modes present in drier sites are non‐random subsets of those present in sites with higher humidity levels. Because reproductive modes are phylogenetically conserved among amphibians, sites with a greater number of reproductive modes supported greater phylogenetic diversity. Sites with high precipitation throughout the year provided suitable environmental conditions for a larger number of reproductive modes, whereas sites with low precipitation and typical seasonal climates supported only those reproductive modes specialized to resist desiccation. Main conclusions Our results show that humidity‐related variables are key environmental factors related to both the richness of reproductive modes and phylogenetic diversity. Our results support the hypothesis that the higher phylogenetic diversity found in moister sites reflects differences in the tolerance to desiccation among different reproductive modes. Given that reproductive modes are associated with susceptibility to desiccation, their incorporation into explanatory models may trigger a significant advance in the understanding of the mechanisms regulating the species richness and composition of amphibian communities.     

The evolution of reproductive and genomic diversity in ray-finned fishes: insights from phylogeny and comparative analysis

Collectively, ray-finned fishes (Actinopterygii) display far more diversity in many reproductive and genomic features than any other major vertebrate group. Recent large-scale comparative phylogenetic analyses have begun to reveal the evolutionary patterns and putative causes for much of this diversity. Several such recent studies have offered clues to how different reproductive syndromes evolved in these fishes, as well as possible physiological and genomic triggers. In many cases, repeated independent origins of complex reproductive strategies have been uncovered, probably reflecting convergent selection operating on common suites of underlying genes and hormonal controls. For example, phylogenetic analyses have uncovered multiple origins and predominant transitional pathways in the evolution of alternative male reproductive tactics, modes of parental care and mechanisms of sex determination. They have also shown that sexual selection in these fishes is repeatedly associated with particular reproductive strategies. Collectively, studies on reproductive and genomic diversity across the Actinopterygii illustrate both the strengths and the limitations of comparative phylogenetic approaches on large taxonomic scales.     

A molecular phylogenetic analysis of reproductive trait evolution in the soft coral genus Alcyonium

The soft coral genus Alcyonium is among the most reproductively diverse invertebrate taxa known: The genus includes species that vary both in mode of reproduction (including broadcast spawners, internal brooders, and external brooders) and sexual expression (gonochores, hermaphrodites, and a unisexual parthenogen). Such diversity offers a unique opportunity to examine associations between reproductive and morphological traits in a phylogenetic context. We used an approximately 900-bp sequence of the nuclear ribosomal gene complex spanning the internal transcribed spacer (ITS) regions to construct a molecular phylogeny for 14 European and North American species of Alcyonium onto which we mapped the known distribution of reproductive and morphological traits. The phylogeny suggests that hermaphroditism or parthenogenesis has evolved independently at least twice in this genus, and always in internally brooding species. Broadcast spawning and external brooding only occur in species with large colony size, whereas all species with small colony size brood their larvae internally. Internal brooding and small size appear to be ancestral in this genus; if this is the case, an association between broadcast spawning and large colony size has evolved independently in at least two clades. This tendency of small adults to brood their larvae while large adults broadcast spawn them into the plankton has been observed in a variety of solitary invertebrate taxa, but to date has not been documented in any other colonial invertebrates. Moreoever, it has been suggested that organisms with a colonial growth form should not experience the allometric constraints on brood space that have been proposed to explain the association between adult size and mode of reproduction in solitary organisms. Unlike many other colonial groups, however, module (polyp) size is strongly correlated with colony size in Alcyonium, and constraints on brooding may be imposed by module, rather than colony, allometry. The very close genetic relationship (< 1% sequence divergence) and shared polymorphisms among A. digitatum (a large, gonochoric broadcast spawner), A. siderium, and A. sp. A (intermediate-sized and small hermaphroditic, internal brooders) suggest that evolutionary transitions between broadcast spawning and brooding and between gonochorism and hermaphroditism can occur easily and rapidly in this group.     

The evolution of parental care and egg size: a comparative analysis in frogs

The evolution of parental care and egg size has attracted considerable attention and theoretical debate. Several different hypotheses have been proposed concerning the trajectories of parental care and egg size evolution and the order of specific evolutionary transitions. Few comparative studies have investigated the predictions of these hypotheses. Here, we investigate the evolutionary association between parental care and egg size in frogs in a phylogenetic context. Data on egg size and presence or absence of parental care in various species of frogs was gathered from the scientific literature. As a basis for our comparative analyses, we developed a phylogenetic supertree, by combining the results of multiple phylogenetic analyses in the literature using matrix representation parsimony. Using phylogenetic pairwise comparisons we demonstrated a significant association between the evolution of parental care and large egg size. We then used recently developed maximum likelihood methods to infer the evolutionary order of specific transitions. This analysis revealed that the evolution of large egg size typically precedes the evolution of parental care, rather than the reverse. We discuss the relevance of our results to previous hypotheses concerning the evolution of parental care and egg size.     

The evolution of partial reproductive isolation as an adaptive optimum

Decades of theoretical work on the evolution of adaptive prezygotic isolation have led to an interesting finding—namely that stable partial reproductive isolation is a relatively common outcome. This conclusion is generally lost, however, in the desire to pinpoint when exactly speciation occurs. Here, we argue that the evolution of partial reproductive isolation is of great interest in its own right and matches empirical findings that ongoing hybridization is taxonomically widespread. We present the mechanisms by which partial reproductive isolation can be a stable evolutionary endpoint, concentrating on insights from theoretical studies. We focus not on cases in which hybridization results from constraints imposed by ongoing migration or mutation, but on the intriguing idea that partial reproductive isolation may instead be an adaptive optimum. We identify three general categories of selective mechanisms that can lead to partial reproductive isolation: context-dependent hybrid advantage, indirect selection due to the varying actions of sexual selection in different geographic contexts, and a balance of costs of choosiness with indirect selection for stronger mating preferences. By any of these mechanisms, stable partial reproductive isolation can potentially provide a robust evolutionary alternative to either complete speciation or population fusion.     

The evolution of reproductive isolation in the ectomycorrhizal Hebeloma crustuliniforme aggregate (Basidiomycetes) in northwestern Europe: a phylogenetic approach

Abstract. To reconstruct the evolution of reproductive isolation in the ectomycorrhizal Hebeloma crustuliniforme aggregate (Basidiomycetes), phylogenetic relationships were determined between strains that belong to a clade consisting of nine intercompatibility groups (ICGs, biological species). Four of these nine ICGs are partially compatible and belong to the H. crustuliniforme aggregate. Different levels of partial compatibility have been found between these four ICGs. Between ICGs 3 and 4, 15% of the combinations were compatible. One strain was compatible with all isolates of both ICGs 3 and 4 and also with one isolate of ICG 2. Both a nuclear phylogeny, based on ribosomal IGS sequence data, and a mitochondrial phylogeny, based on a group-I intron located in the large subunit ribosomal RNA gene (LrRNA), were reconstructed. The level of incompatibility was compared with the phylogenetic history of individuals belonging to this clade.
Different relationships were found between the level of compatibility and the relative age of the most recent common ancestor (MRCA) for different ICGs. On the one hand, the evolution of incompatibility between ICGs 2 and 3/4 is most consistent with the class of "divergence- first" models because a positive correlation was found between the relative age of the MRCA and the level of incompatibility for ICG 2 versus 3/4. On the other hand, the lack of such a correlation for ICGs 3 and 4 shows that (partial) incompatibility between these ICGs has arisen without strong divergence. The ecological (and to a lesser extent geographical) differences found between ICGs 3 and 4 suggest that selection for incompatibility, associated with host tree preference, has been important in the evolution of incompatibility between these two ICGs. The incongruence between the nuclear and mitochondrial trees for ICG 1 could be explained by a hybrid origin of this ICG, with different donors of the mitochondrial and nuclear sequences.     

Extreme plasticity in reproductive biology of an oviparous lizard

Most oviparous squamate reptiles lay their eggs when embryos have completed less than one‐third of development, with the remaining two‐thirds spent in an external nest. Even when females facultatively retain eggs in dry or cold conditions, such retention generally causes only a minor (<10%) decrease in subsequent incubation periods. In contrast, we found that female sand lizards (Lacerta agilis) from an experimentally founded field population (established ca. 20 years ago on the southwest coast of Sweden) exhibited wide variation in incubation periods even when the eggs were kept at standard (25°C) conditions. Females that retained eggs in utero for longer based on the delay between capture and oviposition produced eggs that hatched sooner. In the extreme case, eggs hatched after only 55% of the “normal” incubation period. Although the proximate mechanisms underlying this flexibility remain unclear, our results from this first full field season at the new study site show that females within a single cold‐climate population of lizards can span a substantial proportion of the continuum from “normal” oviparity to viviparity.     

Male-male competition and repeated evolution of terrestrial breeding in Atlantic Coastal Forest frogs*

Terrestrial breeding is a derived condition in frogs, with multiple transitions from an aquatic ancestor. Shifts in reproductive mode often involve changes in habitat use, and these are typically associated with diversification in body plans, with repeated transitions imposing similar selective pressures. We examine the diversification of reproductive modes, male and female body sizes, and sexual size dimorphism (SSD) in the Neotropical frog genera Cycloramphus and Zachaenus, both endemic to the Atlantic rainforest of Brazil. Species in this clade either breed in rocky streams (saxicolous) or in terrestrial environments, allowing us to investigate reproductive habitat shifts. We constructed a multilocus molecular phylogeny and inferred evolutionary histories of reproductive habitats, body sizes, and SSD. The common ancestor was small, saxicolous, and had low SSD. Terrestrial breeding evolved independently three times and we found a significant association between reproductive habitat and SSD, with shifts to terrestrial breeding evolving in correlation with decreases in male body size, but not female body size. Terrestrial breeding increases the availability of breeding sites and results in concealment of amplexus, egg-laying, and parental care, therefore reducing male-male competition at all stages of reproduction. We conclude that correlated evolution of terrestrial reproduction and small males is due to release from intense male-male competition that is typical of exposed saxicolous breeding.     

The evolution of reproductive strategies in dasyurid marsupials: implications of molecular phylogeny

Dasyurid marsupials show a remarkable diversity of reproductive patterns ranging from aseasonal polyoestry to restricted annual breeding in which males synchronously die after a brief mating season. Previous studies have categorized dasyurid reproduction into six strategies, defined on the basis of five life-history characters. We provide an up-to-date summary of reproductive traits in dasyurid species and examine the evolution of these characters on a phylogeny for the family recently obtained from DNA sequence data. Our results suggest that reproductive evolution in modern dasyurids is characterized by a basal separation of subfamily lineages employing Strategy II (monoestrous females, restricted breeding season, 11 months to maturity; Dasyurinae) and Strategy V (polyoestrous females, extended breeding season, 8–11 months to maturity; Sminthopsinae). Strategies I (male die-off) and III (facultative polyoestry) appear to have arisen several times from Strategy II or V ancestors, and Strategy IV appears to have arisen within Sminthopsis from a Strategy V ancestor. Strategy VI (aseasonal breeding) has arisen independently in each of the four major dasyurid lineages (tribes), and is highly (but not perfectly) correlated with New Guinean endemism. This scenario is not strongly affected if reproductive characters are optimized on an alternative phylogeny more consistent with morphology-based opinions on species relationships. When evaluated in light of current habitat associations and geographic distributions, the reproductive data suggest that the Miocene diversification of modern dasyurids may have been correlated with the invasion of dry forest or woodland habitats.     

The evolution of daily food sharing: A Bayesian phylogenetic analysis

Some human subsistence economies are characterized by extensive daily food sharing networks, which may buffer the risk of shortfalls and facilitate cooperative production and divisions of labor among households. Comparative studies of human food sharing can assess the generalizability of this theory across time, space, and diverse lifeways. Here we test several predictions about daily sharing norms–which presumably reflect realized cooperative behavior–in a globally representative sample of nonindustrial societies (the Standard Cross-Cultural Sample), while controlling for multiple sources of autocorrelation among societies using Bayesian multilevel models. Consistent with a risk-buffering function, we find that sharing is less likely in societies with alternative means of smoothing production and consumption such as animal husbandry, food storage, and external trade. Further, food sharing was tightly linked to labor sharing, indicating gains to cooperative production and perhaps divisions of labor. We found a small phylogenetic signal for food sharing (captured by a supertree of human populations based on genetic and linguistic data) that was mediated by food storage and social stratification. Food sharing norms reliably emerge as part of cooperative economies across time and space but are culled by innovations that facilitate self-reliant production.     

A cladistic phylogeny of the genus Littorina (Gastropoda): implications for evolution of reproductive strategies and for classification

Gross anatomical characters of all 18 species of Littorina are used to construct a phylogenetic hypothesis for the genus, by the method of cladistic analysis. The resulting cladogram suggests that of the four subgenera of Littorina, one (Littorina) is paraphyletic. It is uncertain whether the genus Mainwaringia should be included in Littorina. It is shown that the non-planktotrophic Littorina species in the northern Atlantic comprise a monophyletic group, with the sister-species L. kurila and/or L. subrotundata in the northern Pacific. Invasion of the Atlantic by a minimum of two Pacific species, across the Arctic migration route established during the late Cenozoic, is sufficient to account for the modern distribution of the subgenera Littorina and Neritrema. The importance of the cladogram as a basis for hypotheses of adaptation is illustrated by a discussion of spawn and development in Littorina.     

Infanticide in the evolution of reproductive synchrony: effects on reproductive success

Synchronous breeding in animals and plants has stimulated both a theoretical and empirical examination of the possible benefits of active synchronization. The selective pressures of predation and infanticide are the strongest candidates proposed to explain the evolution of reproductive synchrony. Alternatively, breeding asynchronously with conspecifics may ensure a greater availability of resources per breeder. However, the possible fitness benefits resulting from active asynchronization have not yet received attention in evolutionary ecology. Here we present a hypothesis, based on a graphical model, illustrating the costs and benefits of the two modes of reproduction. We tested the hypothesis empirically using a 2 x 2 full factorial study design, where reproductive synchrony and infanticide tactics were manipulated in enclosed populations of the bank vole. The results reveal a relationship between infanticide tactics and breeding synchrony as illustrated by our hypothesis. In general, female reproductive success (number and size of offspring surviving to weaning) was significantly lower in infanticidal populations. Moreover, an asynchronous breeding pattern proved to be advantageous in the noninfanticidal population but this advantage of asynchrony was lost as infanticide became common in the population. Our findings support the idea that synchronous reproduction could have evolved as a counterstrategy against infanticide.     

Effects of fire on bird diversity and abundance in an East African savanna

Fire is an important determinant of many aspects of savanna ecosystem structure and function. However, relatively little is known about the effects of fire on faunal biodiversity in savannas. We conducted a short‐term study to examine the effects of a replicated experimental burn on bird diversity and abundance in savanna habitat of central Kenya. Twenty‐two months after the burn, Shannon diversity of birds was 32% higher on plots that had been burned compared with paired control plots. We observed no significant effects of burning on total bird abundance or species richness. Several families of birds were found only on plots that had been burned; one species, the rattling cisticola (Cisticola chiniana), was found only on unburned plots. Shrub canopy area was negatively correlated with bird diversity on each plot, and highly correlated with grass height and the abundance of orthopterans. Our results suggest that the highest landscape‐level bird diversity might be obtained through a mosaic of burned and unburned patches. This is also most likely to approximate the historical state of bird diversity in this habitat, because patchy fires have been an important natural disturbance in tropical ecosystems for millennia.     

The evolution of an annual life cycle in killifish: adaptation to ephemeral aquatic environments through embryonic diapause

An annual life cycle is characterized by growth, maturity, and reproduction condensed into a single, short season favourable to development, with production of embryos (seeds, cysts, or eggs) capable of surviving harsh conditions which juveniles or adults cannot tolerate. More typically associated with plants in desert environments, or temperate‐zone insects exposed to freezing winters, the evolution of an annual life cycle in vertebrates is fairly novel. Killifish, small sexually dimorphic fishes in the Order Cyprinodontiformes, have adapted to seasonally ephemeral water bodies across much of Africa and South America through the independent evolution of an annual life history. These annual killifish produce hardy desiccation‐resistant eggs that undergo diapause (developmental arrest) and remain buried in the soil for long periods when fish have perished due to the drying of their habitat. Killifish are found in aquatic habitats that span a continuum from permanent and stable to seasonal and variable, thus providing a useful system in which to piece together the evolutionary history of this life cycle using natural comparative variation. I first review adaptations for life in ephemeral aquatic environments in killifish, with particular emphasis on the evolution of embryonic diapause. I then bring together available evidence from a variety of approaches and provide a scenario for how this annual life cycle evolved. There are a number of features within Aplocheiloidei killifish including their inhabitation of marginal or edge aquatic habitat, their small size and rapid attainment of maturity, and egg properties that make them particularly well suited to the colonization of ephemeral waters.