skip to main content


The NSF Public Access Repository (NSF-PAR) system and access will be unavailable from 10:00 PM ET on Friday, December 8 until 2:00 AM ET on Saturday, December 9 due to maintenance. We apologize for the inconvenience.

Title: Ultrastructural variation and adaptive evolution of the ovipositor in the endemic Hawaiian Drosophilidae

Ecological diversification of the endemic Hawaiian Drosophilidae has been accompanied by striking divergence in egg morphology, and ovarian structure and function. To determine how these flies successfully oviposit in a variety of breeding substrates, we used Scanning Electron Microscopy to examine the ultrastructure of the ovipositor of a sample of 65Drosophilaspecies and fiveScaptomyzaspecies of this hyperdiverse monophyletic group. TheDrosophilaspecies analyzed included representatives of the fungus‐breedinghaleakalaegroup, the leaf‐breedingantopocerusand modified tarsus groups, the modified mouthparts species group, thenudidrosophila, and the picture wing clade; the latter sample of 41 species from four species groups included stem‐ and bark‐breeders, as well as tree sap flux‐breeders. Ovipositor length was found to vary more than 12‐fold among Hawaiian drosophilids, with the longest ovipositors observed in the bark‐breeding species and the shortest among theScaptomyzaand fungus‐breeders. More noteworthy is the striking variation in overall shape and proportions of the ovipositor, in the shape of the apical region, and in the pattern of sensory structures or ovisensilla. Ultrastructural observations of the pair of long subapical sensilla on the ventral side identify these, for the first time, as taste bristles. Ovipositor form correlates strongly with the oviposition substrate used by the species, being of a distinctive shape and size in each case. We infer that the observed morphological divergence in the ovipositor is adaptive and the product of natural selection for successful reproduction in alternate microhabitats. The array of ovipositor forms that have evolved among the HawaiianDrosophilaspecies represent a series of ecomorphs that along with other divergent traits of the female reproductive system, have contributed to the successful adaptive radiation of this remarkable fauna.

more » « less
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  ;  
Publisher / Repository:
Wiley Blackwell (John Wiley & Sons)
Date Published:
Journal Name:
Journal of Morphology
Page Range / eLocation ID:
p. 1725-1752
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Societal Impact Statement

    Fleshy fruits provide humans with many flavorful and nutritious crops. Understanding the diversity of these plants is fundamental to managing agriculture and food security in a changing world. This study surveyed fruit trait variation across species of tomato wild relatives and explored associations among color, size, shape, sugars, and acids. These wild tomato species native to South America can be interbred with the economically important cultivated tomato. Beyond its application to tomatoes, deepening our knowledge of how fruit traits evolve together is valuable to crop improvement efforts aimed at breeding more nutritious and appealing varieties of fruits.


    Fleshy fruits display a striking diversity of traits, many of which are important for agriculture. The evolutionary drivers of this variation are not well understood, and most studies have relied on variation found in the wild. Few studies have explored this question on a fine‐grained scale with a group of recently diverged species while controlling for environmental effects.

    We developed the tomato clade as a novel system for fruit trait evolution research by presenting the first common garden‐based systematic survey of variation and phylogenetic signal in color, nutrition, and morphology traits across all 13 species of tomato wild relatives (Solanum sect.Lycopersicon). We laid the groundwork for further testing of potential evolutionary drivers by assessing patterns of clustering and correlation among disperser‐relevant fruit traits as well as historical climate variables.

    We found evidence of two distinct clusters of associated fruit traits defined by color, sugar type, and malic acid concentration. We also observed correlations between a fruit's external appearance and internal nutrient content that could function as honest signals to dispersers. Analyses of historical climate and soil variables revealed an association between red/orange/yellow fruits and high annual average temperature.

    Our results establish the tomato clade as a promising system for testing hypotheses on the drivers of divergence behind early‐stage fleshy fruit evolution, particularly selective pressure from frugivores.

    more » « less
  2. Abstract

    In cooperatively breeding species, subordinates forgo reproduction to assist breeders in raising offspring. When cooperative breeding is facultative, breeders from the same population may differ in whether they are assisted by non‐breeding helpers. Predation risk is a major source of nest failure and assistance during nest defense is often an overlooked, yet important, way helpers assist breeders. A breeder's aggressive response to a nest predator could have important implications for whether they form cooperatively breeding groups. We investigated the hypothesis that breeder aggression toward a nest predator is related to current and future helper recruitment. We tested the prediction that less aggressive breeders were more likely to form cooperative groups, which could occur if these breeders benefit from helper assistance during nest defense. We also considered the possibility that more aggressive breeders were more likely to form cooperative groups. We assessed the effects of partnerships and tested whether aggression exhibited by breeding partners was correlated. We conducted this work in the facultative, cooperatively breeding brown‐headed nuthatch (Sitta pusilla). We measured breeder aggression in response to a taxidermy model of a nest predator to determine whether breeders’ aggression correlated with their current or future helper recruitment. We found no evidence of a sex difference in aggression among breeders and aggression scores of breeding partners were not significantly correlated. Aggression scores for both breeding males and breeding females were unrelated to whether they formed cooperative groups in the current year. We followed most of the breeding males, though not breeding females, across years and found that breeding males’ aggression scores were unrelated to helper recruitment the following year. Our results suggest that breeders’ responses to nest predators are not related to cooperative group formation in this species and that males and females showed comparable levels of aggression toward a nest predator.

    more » « less
  3. Abstract

    Age‐related variation in reproductive performance in long‐lived iteroparous vertebrate species is common, with performance being influenced by within‐individual processes, such as improvement and senescence, in combination with among‐individual processes, such as selective appearance and disappearance. Few studies of age‐related reproductive performance have compared the role of these drivers within a metapopulation, subject to varying degrees of resource competition.

    We accounted for within‐ and among‐individual changes among known‐aged Adélie penguinsPygoscelis adeliaeduring 17 years (1997–2013), at three clustered colonies of disparate size, to understand patterns in age‐related reproductive success during early and late adulthood.

    Age at first reproduction (AFR) was lowest, and number of breeding attempts highest, at the largest colony. Regardless of AFR, success improved with early post‐recruitment experience. For both oldest and youngest recruitment groups, peak performance occurred at the end of their reproductive life span indicating a possible cost of reproduction. Intermediate recruitment groups reached peak performance in their mid‐reproductive life span and with intermediate breeding experience, before decreasing. Breeding success was lowest for the initial breeding attempt regardless of AFR, but we observed subsequent variation relative to recruitment age. Gaining experience by delaying recruitment positively influenced reproductive performance early in the reproductive life span and was most evident for the youngest breeders. Oldest recruits had the highest initial and peak breeding success. Differences in AFR resulted in trade‐offs in reproductive life span or timing of senescence but not in the overall number of breeding attempts.

    Patterns differed as a function of colony size, and thus competition for resources. Early life improvement in performance at the larger colonies was primarily due to within‐individual factors and at the largest colony, AFR. Regardless of colony size late‐life performance was positively related to the age at last reproduction, indicating selective disappearance of lower performing individuals.

    These results highlight that different life‐history strategies were equally successful, indicating that individuals can overcome potential trade‐offs associated with early‐ and late‐life performance. These results have important implications for understanding the evolution of life‐history strategies responsible for driving population change.

    more » « less
  4. Abstract

    Species interactions shape the evolution of traits, life histories and the pattern of speciation. What is less clear is whether certain types of species interaction are more or less likely to lead to phenotypic divergence among species. We used the brood pollination mutualism between yuccas and yucca moths to test how mutualistic (pollination) and antagonistic (oviposition) traits differ in the propensity to increase phenotypic divergence among pollinator moths. We measured traits of the tentacular mouthparts, structures used by females to actively pollinate flowers, as well as ovipositor traits to examine differences in the rate of evolution of these two suites of traits among pollinator species. Morphological analyses revealed two distinct groups of moths based on ovipositor morphology, but no such groupings were identified for tentacle morphology, even for moths that pollinated distantly related yuccas. In addition, ovipositor traits evolved at significantly faster rates than tentacular traits. These results support theoretical work suggesting that antagonism is more likely than mutualism to lead to phenotypic divergence.

    more » « less
  5. Abstract

    The genusBidens(Compositae) comprisesc. 230 species distributed across five continents, with the 41 Polynesian species displaying the greatest ecomorphological variation in the group. However, the genus has had a long and complicated taxonomic history, and its phylogenetic and biogeographic history are poorly understood. To resolve the evolutionary history of the PolynesianBidens, 152 individuals representing 91 species were included in this study, including 39 of the 41 described species from Polynesia. Four chloroplast and two nuclear DNA markers were utilized to estimate phylogenetic relationships, divergence times, and biogeographic history.Bidenswas found to be polyphyletic withinCoreopsis, consistent with previous assessments. The Polynesian radiation was resolved as monophyletic, with the initial dispersal into the Pacific possibly from South America to either the Hawaiian or Marquesas Islands. From the Marquesas,Bidensdispersed to the Society Islands, and ultimately to the Austral Islands. The initial diversification of the crown group in the Pacific is estimated to have occurred ~1.63 mya (0.74–2.72, 95% HPD), making PolynesianBidensamong the youngest and most rapid plant diversification events documented in the Pacific. Our findings suggest that relatively rare long‐distance dispersal and founder‐event speciation, coupled with subsequent loss of dispersal potential and within‐island speciation, can explain the repeated and explosive adaptive radiation ofBidensthroughout the archipelagoes of Polynesia.

    more » « less