Genetic tests of rapid parallel speciation of flightless birds from an extant volant ancestor

Prior to the extinction wave that followed the human colonization of Oceania, flightless rails (Aves: Rallidae) were among the largest radiations of island birds, and perhaps the most species-rich example of convergent evolution in vertebrates. Insular flightless species are thought to have evolved from extant, volant species that colonized from continental sources and rapidly followed parallel adaptive pathways to flightlessness. The present study provides the first test of this model of speciation using genetic data sampled throughout the range of a putative ancestral species. Mitochondrial control region sequences from 71 individuals of the Gallirallus philippensis species complex reveal essentially no geographic structure within archipelagos and only weak structure among archipelagos, with no major genetic breaks except for birds sampled in the Philippines. Demographic tests of coalescent models support a recent rapid expansion into Oceania (including Australia) out of the Philippines approximately 20 000 years ago. The estimated coalescence of G. philippensis mitochondrial alleles approximately 33 000 years ago closely corresponds to the expansion of humans into the archipelagoes of Near Oceania, suggesting that humans may have facilitated its colonization by exterminating flightless competitors and clearing lowland forests. Phylogenetic analyses that included all G. philippensis haplotypes and samples from 11 single-island endemic flightless species of Gallirallus indicate that G. philippensis is polyphyletic, but is not the ancestor of most of its flightless congeners, as previously thought. Nuclear gene sequences (β-actin inron 3) suggest that G. philippensis polyphyly is at least partly due to hybridization. The flightless condition evolves in rails before reproductive isolation is complete.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 601–616.     

Correlated evolution of female neoteny and flightlessness with male spermatophore production in fireflies (Coleoptera: Lampyridae)

The beetle family Lampyridae (fireflies) encompasses ～100 genera worldwide with considerable diversity in life histories and signaling modes. Some lampyrid males use reproductive accessory glands to produce spermatophores, which have been shown to increase female lifetime fecundity. Sexual dimorphism in the form of neotenic and flightless females is also common in this family. A major goal of this study was to test a hypothesized link between female flight ability and male spermatophore production. We examined macroevolutionary patterns to test for correlated evolution among different levels of female neoteny (and associated loss of flight ability), male accessory gland number (and associated spermatophore production), and sexual signaling mode. Trait reconstruction on a molecular phylogeny indicated that flying females and spermatophores were ancestral traits and that female neoteny increased monotonically and led to flightlessness within multiple lineages. In addition, male spermatophore production was lost multiple times. Our evolutionary trait analysis revealed significant correlations between increased female neoteny and male accessory gland number, as well as between flightlessness and spermatophore loss. In addition, female flightlessness was positively correlated with the use of glows as female sexual signal. Transition probability analysis supported an evolutionary sequence of female flightlessness evolving first, followed by loss of male spermatophores. These results contribute to understanding how spermatophores have evolved and how this important class of seminal nuptial gifts is linked to other traits, providing new insights into sexual selection and life-history evolution.     

Behavioral mutants of Drosophila melanogaster. IV. Analysis of developmentally temperature-sensitive mutations affecting flight

Mutations in 13 genes with temperature-sensitive (ts), flightless phenotypes have been examined. All hop and fly well when raised at the permissive temperature, but fly poorly, or not at all, when raised at the restrictive temperature. The mutations were divided into three groups on the basis of their temperature-sensitive periods (TSPs) for flightlessness. The TSPs for mutations at five loci, fli-C¹, D¹, E¹, I¹, and shak A¹, in the first group are confined to 24 to 48 hr interval during early pupal development. Mutations in the second group, including eag¹⁰¹, fli B¹, and fu^ts1 have continuous TSPs 3 to 4 days in length, extending from late larval through the early pupal stages. The flight TSPs for mutations in the third class, including fli J¹, fli K², flrd H³, and flrd N¹, are almost continuous, and span most of the larval and pupal periods. Many of the mutations have pleiotropic phenotypes, including semilethality and lethality, and wing posture and cuticle abnormalities, with discernible TSPs. One of the more intriguing pleiotropic phenotypes is the ts optomotor response exhibited by fli J², the TSP for which extends from late larval through late pupal stages.     

Patterns of correlated character evolution in flightless birds: a phylogenetic approach

Given a robust phylogeny for a particular higher taxon, it is possible to map the evolution of various character changes onto the phylogeny and study the extent to which they co-occur. Of particular interest are the questions of (a) whether particular morphological changes tend to accompany changes in ecology or behaviour to which they bear a functional relationship and (b) whether changes in those ‘primary’ morphological characters tend to be associated with correlated changes in other aspects of morphology, as would be expected given the high level of morphological integration that characterizes most organisms. Here we report a study of this kind, looking at morphological correlates of the evolution of flightlessness in birds, and using the concentrated changes test to determine whether associations are significant. We find that pectoral reduction, pelvic enlargement and changes in skull morphology significantly co-occur, and that these are usually achieved through heterochrony rather than other kinds of developmental reprogramming. This revised version was published online in November 2006 with corrections to the Cover Date.     

Convergent morphological responses to loss of flight in rails (Aves: Rallidae)

The physiological demands of flight exert strong selection pressure on avian morphology and so it is to be expected that the evolutionary loss of flight capacity would involve profound changes in traits. Here, we investigate morphological consequences of flightlessness in a bird family where the condition has evolved repeatedly. The Rallidae include more than 130 recognized species of which over 30 are flightless. Morphological and molecular phylogenetic data were used here to compare species with and without the ability to fly in order to determine major phenotypic effects of the transition from flighted to flightless. We find statistical support for similar morphological response among unrelated flightless lineages, characterized by a shift in energy allocation from the forelimbs to the hindlimbs. Indeed, flightless birds exhibit smaller sterna and wings than flighted taxa in the same family along with wider pelves and more robust femora. Phylogenetic signal tests demonstrate that those differences are independent of phylogeny and instead demonstrate convergent morphological adaptation associated with a walking ecology. We found too that morphological variation was greater among flightless rails than flighted ones, suggesting that relaxation of physiological demands during the transition to flightlessness frees morphological traits to evolve in response to more varied ecological opportunities.     

Panbiogeography and rails of the genus Gallirallus

Abstract

An investigation of flightlessness in the Rallidae led me to question the theories of Olson (1973); that all rails in the genus Gallirallus were distributed over their present range by recent flighted dispersal; and that flightlessness is a recent process conferred by the paedomorphic process neoteny. The current distribution of some members of Gallirallus (Olson 1973a) are interpreted using the panbiogeographic method of Croizat (1958, 1958a). This method indicates that the distribution of some rails is similar to other biota. I suggest the group may be ancient, and its distribution the result of vicariism. Consequently, the evolution of flightless morphology need not be fast, and the flightless rails on different land masses could be the result of flightless radiations.     

Molecular phylogeny and phylogeography of flightless beetles Parechthistatus gibber and Hayashiechthistatus inexpectus (Coleoptera: Cerambycidae) inferred from mitochondrial COI gene sequences

To elucidate the speciation patterns of two endemic flightless cerambycid beetles, Parechthistatus gibber and Hayashiechthistatus inexpectus, molecular phylogenetic analysis was carried out. A 1144 bp region of the cytochrome oxidase subunit I gene was sequenced for individuals from 51 local populations of these species. There were nine haplotype lineages of P. gibber, and H. inexpectus was included within a P. gibber lineage. These lineages were highly divergent and occurred in different regions. Based on previously published molecular change rates for the COI gene (1.5–2.3% per million years), the time of divergence of P. gibber COI haplotypes was inferred to be 3.0–4.6 million years ago, in the Pliocene.     

The evolution of flightlessness: Is history important?

Summary Though most birds and insects are capable of flight (volant) some species are flightless. In this paper I test the hypothesis that phylogenetic constraints have played a role in the evolution of flightlessness. If speciation occurred after the evolutionary transition to flightlessness, inferences concerning the importance of particular aspects of the environment on the probability of the evolution of flightlessness may be statistically spurious because of the inflation of the sample size. Among birds, ratites and penguins illustrate the phenomenon of considerable speciation subsequent to the transition to the evolution of flightlessness. In contrast, the rails represent a group in which each flightless species probably represents a separate evolutionary transition. There are many more flightless insect species than bird species and several orders are monomorphically flightless, the sometimes enormous speciation within the order following and possibly being a consequence of the evolution of flightlessness. While it can be shown in insects that flightlessness has evolved independently many times, there are at least as many cases in which the question cannot be resolved. Therefore, in both birds and insects phylogenetic effects should not be ignored, for the number of evolutionary transitions may be much less than the number of species. The effect of incorporating phylogenetic (or at least taxonomic) constraints into the analysis of habitat factors associated with flightlessness is considered.     

Species status and population genetic structure of the flightless chafer beetles Prodontria modesta and P. bicolorata (Coleoptera; Scarabaeidae) from South Island, New Zealand

This study uses isozyme electrophoresis to investigate the systematic status of two rare flightless chafer beetle species, Prodontria modesta and P. bicolorata , currently distinguished solely on the basis of colour. Seven polymorphic loci were analysed for the species in sympatry and allopatry. In sympatry, gene frequencies imply no genetic barrier between the two colour forms. Wright's hierarchical F-statistics were calculated to determine how the genetic variation is partitioned across the geographic range of the two species. Strong geographic structuring occurs at the population level but there is little genetic differentiation attributable to species. Comparisons of morphological measurements are in support of the electrophoretic results. The systematic significance of the two distinct colour forms is thus questionable. Under the biological, recognition or phylogenetic species concepts, the genetic data suggest that there is only one species, polytypic for a colour pattern. Most of the genetic diversity of this group of beetles lies within and among populations, which differ quite markedly over their geographic range, rather than between the two named species.