The role of sexual isolation during rapid ecological divergence: evidence for a new dimension of isolation in Rhagoletis pomonella

The pace of divergence and likelihood of complete speciation may depend how and when different types of reproductive barriers evolve. After initial reproductive barriers evolve, questions remain about how subsequently evolving barriers may facilitate additional divergence and potential speciation. We tested for the presence of sexual isolation (reduced mating between populations due to divergent mating preferences and traits) in Rhagoletis pomonella flies, a model system for incipient ecological speciation. We measured the strength of sexual isolation between two very recently diverged (~170 years) sympatric populations, adapted to different host fruits. We found that sexual isolation was significantly stronger than expectations of random mating. Thus, sexual isolation may play an important role in reducing gene flow allowed by earlier-acting ecological barriers. We also found that sexual isolation was markedly asymmetric between the sexes of each population. Lastly, we tested how warmer temperatures predicted under climate change could alter sexual isolation and found that mating interactions were sensitive to temperature experienced during development. Our findings provide a window into the early divergence process and the role of sexual isolation after initial ecological divergence, in addition to examining multiple factors that could shape the likelihood of further divergence.

Gorgonian Responses to Environmental Change on Coral Reefs in SE Sulawesi, Indonesia

<p>Gorgonian corals (Cnidaria: Anthozoa: Octocorallia) are conspicuous, diverse and often dominant components of benthic marine environments. Intra- & interspecific morphological variability in gorgonians are influenced by environmental factors such as light, sedimentation and flow rates. Yet, little is known about the responses of gorgonian taxa to environmental parameters particularly in Indonesia, despite their high regional abundance and diversity. With a burgeoning human population and subsequent marine resource exploitation, reefs throughout the Indonesian archipelago are under rapid decline and often destroyed. Conservation surveys are however, underway with a tendency to overlook gorgonian taxa primarily due to unresolved taxonomic assignment leading to difficulties in field identification. The aims of this study were to: 1) characterise gorgonian diversity and ecology across a gradient of habitat quality within the Wakatobi Marine National Park (WMNP), SE Sulawesi, Indonesia, 2) assess morphological and genetic variability between morphotypes of the ubiquitous zooxanthellate isidid Isis hippuris Linnaeus 1758 from healthy and degraded reefs, 3) determine if I. hippuris morphotypes are environmentally induced (plastic) or genetically derived through reciprocal transplant experiments (RTEs) between contrasting reefs and thus, 4) identify mechanisms of plasticity capacity or divergence through phenotypic trait integration in response to environmental change. Ecological surveys revealed considerable gorgonian diversity with a total of 197 species and morphotypes from 42 genera, and 12 families within the suborders Calcaxonia and Holaxonia and the group Scleraxonia, with current estimates of over 21 new species and 28 new species records for the region. Gorgonian abundance and diversity increased with reef health and bathymetry. However, a clear loss of gorgonian diversity existed with increased sedimentation and reduced light due to anthropogenic disturbance. In particular, two distinct I. hippuris morphotypes were highly abundant between environmental clines: short-branched multi/planar colonies on healthy reefs, and long-branched bushy colonies on degraded reefs. Comparative morphological and molecular analyses using ITS2 sequence and predicted secondary structure, further corroborated haplotype differences relative to morphotypes between environments. However, unsatisfactory assignment of I. hippuris morphotypes to previously described alternatives (Isis reticulata Nutting 1910, Isis minorbrachyblasta Zou, Huang & Wang 1991) questions the validity to such taxonomic assignments. Phylogenetic analyses also confirm that the polyphyletic nature of the Isididae lies in its type species I. hippuris, being unrelated to the rest of its family members. A one-year RTE revealed three key results, that: 1) reduced survivorship of healthy reef morphotypes on degraded reefs implied the onset of lineage segregation through immigrant inviability, 2) prominent phenotypic traits were at the morphological and bio-optical levels revealing high phenotypic plasticity in healthy clones, and relative insensitivity to environmental change in degraded reef morphotypes, indicative of local adaptation leading to incipient ecological divergence, and 3) photoacclimation at the bio-optical level was not attributed to endosymbiont diversity or shuffling, with all test colonies possessing a novel clade D1a Symbiodinium. While it is clear that gorgonian taxa within the WMNP are of exceptional diversity and abundance, responses to environmental perturbation highlight three pertinent, testable ideas. Firstly, increased species richness specifically with depth in azooxanthellate taxa, invite tests of deep-reef refugia previously established through geological change. Secondly, ecological assessment targets research on informative taxa for focused systematics and mechanisms of phenotypic divergence. Thirdly, exploring intrinsic and extrinsic interactions that define the host-symbiont relationship and differential biological success using physiological and next generation sequencing approaches. These objectives would provide considerable insight into the evolutionary processes to environmental change, accelerated by anthropogenic encroachment. Taken together, this work signifies that gorgonian corals within the WMNP are of foremost diversity and concern, exhibiting informative ecological and mechanistic responses to environmental perturbation. This evidence elicits tests of deep-reef refugia, priority systematics, mechanisms of ecological divergence and physiological assessment. Such tests inevitably expand our understanding of the intrinsic and extrinsic associations of gorgonian taxa to environmental change from an historical and predictive perspective yielding benefits to conservation assessment and management.</p>

Gorgonian Responses to Environmental Change on Coral Reefs in SE Sulawesi, Indonesia

<p>Gorgonian corals (Cnidaria: Anthozoa: Octocorallia) are conspicuous, diverse and often dominant components of benthic marine environments. Intra- & interspecific morphological variability in gorgonians are influenced by environmental factors such as light, sedimentation and flow rates. Yet, little is known about the responses of gorgonian taxa to environmental parameters particularly in Indonesia, despite their high regional abundance and diversity. With a burgeoning human population and subsequent marine resource exploitation, reefs throughout the Indonesian archipelago are under rapid decline and often destroyed. Conservation surveys are however, underway with a tendency to overlook gorgonian taxa primarily due to unresolved taxonomic assignment leading to difficulties in field identification. The aims of this study were to: 1) characterise gorgonian diversity and ecology across a gradient of habitat quality within the Wakatobi Marine National Park (WMNP), SE Sulawesi, Indonesia, 2) assess morphological and genetic variability between morphotypes of the ubiquitous zooxanthellate isidid Isis hippuris Linnaeus 1758 from healthy and degraded reefs, 3) determine if I. hippuris morphotypes are environmentally induced (plastic) or genetically derived through reciprocal transplant experiments (RTEs) between contrasting reefs and thus, 4) identify mechanisms of plasticity capacity or divergence through phenotypic trait integration in response to environmental change. Ecological surveys revealed considerable gorgonian diversity with a total of 197 species and morphotypes from 42 genera, and 12 families within the suborders Calcaxonia and Holaxonia and the group Scleraxonia, with current estimates of over 21 new species and 28 new species records for the region. Gorgonian abundance and diversity increased with reef health and bathymetry. However, a clear loss of gorgonian diversity existed with increased sedimentation and reduced light due to anthropogenic disturbance. In particular, two distinct I. hippuris morphotypes were highly abundant between environmental clines: short-branched multi/planar colonies on healthy reefs, and long-branched bushy colonies on degraded reefs. Comparative morphological and molecular analyses using ITS2 sequence and predicted secondary structure, further corroborated haplotype differences relative to morphotypes between environments. However, unsatisfactory assignment of I. hippuris morphotypes to previously described alternatives (Isis reticulata Nutting 1910, Isis minorbrachyblasta Zou, Huang & Wang 1991) questions the validity to such taxonomic assignments. Phylogenetic analyses also confirm that the polyphyletic nature of the Isididae lies in its type species I. hippuris, being unrelated to the rest of its family members. A one-year RTE revealed three key results, that: 1) reduced survivorship of healthy reef morphotypes on degraded reefs implied the onset of lineage segregation through immigrant inviability, 2) prominent phenotypic traits were at the morphological and bio-optical levels revealing high phenotypic plasticity in healthy clones, and relative insensitivity to environmental change in degraded reef morphotypes, indicative of local adaptation leading to incipient ecological divergence, and 3) photoacclimation at the bio-optical level was not attributed to endosymbiont diversity or shuffling, with all test colonies possessing a novel clade D1a Symbiodinium. While it is clear that gorgonian taxa within the WMNP are of exceptional diversity and abundance, responses to environmental perturbation highlight three pertinent, testable ideas. Firstly, increased species richness specifically with depth in azooxanthellate taxa, invite tests of deep-reef refugia previously established through geological change. Secondly, ecological assessment targets research on informative taxa for focused systematics and mechanisms of phenotypic divergence. Thirdly, exploring intrinsic and extrinsic interactions that define the host-symbiont relationship and differential biological success using physiological and next generation sequencing approaches. These objectives would provide considerable insight into the evolutionary processes to environmental change, accelerated by anthropogenic encroachment. Taken together, this work signifies that gorgonian corals within the WMNP are of foremost diversity and concern, exhibiting informative ecological and mechanistic responses to environmental perturbation. This evidence elicits tests of deep-reef refugia, priority systematics, mechanisms of ecological divergence and physiological assessment. Such tests inevitably expand our understanding of the intrinsic and extrinsic associations of gorgonian taxa to environmental change from an historical and predictive perspective yielding benefits to conservation assessment and management.</p>

Copy number variation of a fatty acid desaturase gene Fads2 associated with ecological divergence in freshwater stickleback populations

Fitness of aquatic animals can be limited by the scarcity of nutrients such as long-chain polyunsaturated fatty acids, especially docosahexaenoic acid (DHA). DHA availability from diet varies among aquatic habitats, imposing different selective pressures on resident animals to optimize DHA acquisition and synthesis. For example, DHA is generally poor in freshwater ecosystems compared to marine ecosystems. Our previous work revealed that, relative to marine fishes, several freshwater fishes evolved higher copy numbers of the fatty acid desaturase2 ( Fads2 ) gene, which encodes essential enzymes for DHA biosynthesis, likely compensating for the limited availability of DHA in freshwater. Here, we demonstrate that Fads2 copy number also varies between freshwater sticklebacks inhabiting lakes and streams with stream fish having higher Fads2 copy number. Additionally, populations with benthic-like morphology possessed higher Fads2 copy number than those with planktivore-like morphology. This may be because benthic-like fish mainly feed on DHA-deficient prey such as macroinvertebrates whereas planktivore-like fish forage more regularly on DHA-rich prey, like copepods. Our results suggest that Fads2 copy number variation arises from ecological divergence not only between organisms exploiting marine and freshwater habitats but also between freshwater organisms exploiting divergent resources.

Ecological Divergence Within the Enterobacterial Genus Sodalis: From Insect Symbionts to Inhabitants of Decomposing Deadwood

The bacterial genus Sodalis is represented by insect endosymbionts as well as free-living species. While the former have been studied frequently, the distribution of the latter is not yet clear. Here, we present a description of a free-living strain, Sodalis ligni sp. nov., originating from decomposing deadwood. The favored occurrence of S. ligni in deadwood is confirmed by both 16S rRNA gene distribution and metagenome data. Pangenome analysis of available Sodalis genomes shows at least three groups within the Sodalis genus: deadwood-associated strains, tsetse fly endosymbionts and endosymbionts of other insects. This differentiation is consistent in terms of the gene frequency level, genome similarity and carbohydrate-active enzyme composition of the genomes. Deadwood-associated strains contain genes for active decomposition of biopolymers of plant and fungal origin and can utilize more diverse carbon sources than their symbiotic relatives. Deadwood-associated strains, but not other Sodalis strains, have the genetic potential to fix N2, and the corresponding genes are expressed in deadwood. Nitrogenase genes are located within the genomes of Sodalis, including S. ligni, at multiple loci represented by more gene variants. We show decomposing wood to be a previously undescribed habitat of the genus Sodalis that appears to show striking ecological divergence.

A reversal in sensory processing accompanies ongoing ecological divergence and speciation in Rhagoletis pomonella

Changes in behaviour often drive rapid adaptive evolution and speciation. However, the mechanistic basis for behavioural shifts is largely unknown. The tephritid fruit fly Rhagoletis pomonella is an example of ecological specialization and speciation in action via a recent host plant shift from hawthorn to apple. These flies primarily use specific odours to locate fruit, and because they mate only on or near host fruit, changes in odour preference for apples versus hawthorns translate directly to prezygotic reproductive isolation, initiating speciation. Using a variety of techniques, we found a reversal between apple and hawthorn flies in the sensory processing of key odours associated with host fruit preference at the first olfactory synapse, linking changes in the antennal lobe of the brain with ongoing ecological divergence. Indeed, changes to specific neural pathways of any sensory modality may be a broad mechanism for changes in animal behaviour, catalysing the genesis of new biodiversity.

Leucostegia amplissima, the Third Species of the Genus (Hypodematiaceae)

Leucostegia has been long recognized as a small fern genus with only two species, L. immersa and L. pallida. Here we elevate a variety of L. immersa to species level and make the new combination Leucostegia amplissima based on morphological and molecular phylogenetic evidence. Morphologically, Leucostegia amplissima differs from L. immersa by having larger evergreen fronds, smaller indusia, and glandular hairs on the basal stipes. The study of Taiwanese populations further suggested an ecological divergence between L. immersa and L. amplissima.