skip to main content


Title: Shedding light: a phylotranscriptomic perspective illuminates the origin of photosymbiosis in marine bivalves
Abstract Background

Photosymbiotic associations between metazoan hosts and photosynthetic dinoflagellates are crucial to the trophic and structural integrity of many marine ecosystems, including coral reefs. Although extensive efforts have been devoted to study the short-term ecological interactions between coral hosts and their symbionts, long-term evolutionary dynamics of photosymbiosis in many marine animals are not well understood. Within Bivalvia, the second largest class of mollusks, obligate photosymbiosis is found in two marine lineages: the giant clams (subfamily Tridacninae) and the heart cockles (subfamily Fraginae), both in the family Cardiidae. Morphologically, giant clams show relatively conservative shell forms whereas photosymbiotic fragines exhibit a diverse suite of anatomical adaptations including flattened shells, leafy mantle extensions, and lens-like microstructural structures. To date, the phylogenetic relationships between these two subfamilies remain poorly resolved, and it is unclear whether photosymbiosis in cardiids originated once or twice.

Results

In this study, we establish a backbone phylogeny for Cardiidae utilizing RNASeq-based transcriptomic data from Tridacninae, Fraginae and other cardiids. A variety of phylogenomic approaches were used to infer the relationship between the two groups. Our analyses found conflicting gene signals and potential rapid divergence among the lineages. Overall, results support a sister group relationship between Tridacninae and Fraginae, which diverged during the Cretaceous. Although a sister group relationship is recovered, ancestral state reconstruction using maximum likelihood-based methods reveals two independent origins of photosymbiosis, one at the base of Tridacninae and the other within a symbiotic Fraginae clade.

Conclusions

The newly revealed common ancestry between Tridacninae and Fraginae brings a possibility that certain genetic, metabolic, and/or anatomical exaptations existed in their last common ancestor, which promoted both lineages to independently establish photosymbiosis, possibly in response to the modern expansion of reef habitats.

 
more » « less
NSF-PAR ID:
10225768
Author(s) / Creator(s):
; ; ; ; ;
Publisher / Repository:
Springer Science + Business Media
Date Published:
Journal Name:
BMC Evolutionary Biology
Volume:
20
Issue:
1
ISSN:
1471-2148
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract Aim

    We sought to illuminate the history of the arachnid orders Schizomida and Uropygi, neither of which have previously been subjected to global molecular phylogenetic and biogeographical analyses.

    Location

    Specimens used in this study were collected in all major tropical and subtropical areas where they are presently found, including the Americas, Africa, Australia and the Indo‐Pacific region.

    Methods

    From field‐collected specimens, we sequenced two nuclear and two mitochondrial markers, combined these with publicly available data, and conducted multi‐gene phylogenetic analyses on 240 Schizomida, 24 Uropygi and 12 other arachnid outgroups. Schizomid specimens included one specimen from the small family Protoschizomidae; other schizomid specimens were in Hubbardiidae, subfamily Hubbardiinae, which holds 289 of the order's 305 named species. We inferred ancestral areas using the Dispersal‐Extinction‐Cladogenesis model of range evolution, and we used fossil calibrations to estimate divergence times.

    Results

    We recovered monophyletic Schizomida and Uropygi as each other's sister group, forming the clade Thelyphonida, and terminals from the New World were usually positioned as the earliest diverging lineages. The ancestral area for schizomids reconstructed unambiguously to the region comprised of Mexico, Southern California and Florida (the xeric New World subtropics). Optimal trees suggested a single colonization of the Indo‐Pacific in both orders, although this did not receive bootstrap support. Molecular dating gave an Upper Carboniferous origin for each order, and a mid‐Cretaceous expansion of Schizomida, including the origin and initial diversification of those in the Indo‐Pacific.

    Main conclusions

    Ancestral area reconstructions, molecular dating and fossil evidence all support an Upper Carboniferous, tropical Pangean origin for Thelyphonida, Schizomida and perhaps Uropygi. Much of this region became unsuitable habitat for these arachnids during the breakup of Pangea, but they persisted in the area that is now Meso‐ and South America. From there they then expanded to the Indo‐Pacific, where schizomids today display an idiosyncratic combination of microendemism and long‐range dispersal.

     
    more » « less
  2. Abstract

    Bacterial symbionts are integral to the health and homeostasis of invertebrate hosts. Notably, members of the Rickettsiales genus Wolbachia influence several aspects of the fitness and evolution of their terrestrial hosts, but few analogous partnerships have been found in marine systems. We report here the genome, phylogenetics, and biogeography of a ubiquitous and novel Rickettsiales species that primarily associates with marine organisms. We previously showed that this bacterium was found in scleractinian corals, responds to nutrient exposure, and is associated with reduced host growth and increased mortality. This bacterium, like other Rickettsiales, has a reduced genome indicative of a parasitic lifestyle. Phylogenetic analysis places this Rickettsiales within a new genus we define as “Candidatus Aquarickettsia.” Using data from the Earth Microbiome Project and SRA databases, we also demonstrate that members of “Ca. Aquarickettsia” are found globally in dozens of invertebrate lineages. The coral-associated “Candidatus A. rohweri” is the first finished genome in this new clade. “Ca. A. rohweri” lacks genes to synthesize most sugars and amino acids but possesses several genes linked to pathogenicity including Tlc, an antiporter that exchanges host ATP for ADP, and a complete Type IV secretion system. Despite its inability to metabolize nitrogen, “Ca. A. rohweri” possesses the NtrY-NtrX two-component system involved in sensing and responding to extracellular nitrogen. Given these data, along with visualization of the parasite in host tissues, we hypothesize that “Ca. A. rohweri” reduces coral health by consuming host nutrients and energy, thus weakening and eventually killing host cells. Last, we hypothesize that nutrient enrichment, which is increasingly common on coral reefs, encourages unrestricted growth of “Ca. A. rohweri” in its host by providing abundant N-rich metabolites to be scavenged.

     
    more » « less
  3. Premise

    We take an integrative approach in assessing how introgression and Pleistocene climate fluctuations have shaped the diversification of the coreLentagoclade ofViburnum, a group of five interfertile species with broad areas of sympatry. We specifically tested whether flowering time plays a role in maintaining species isolation.

    Methods

    RAD‐seq data for 103 individuals were used to infer the species relationships and the genetic structure within each species. Flowering times were compared among species on the basis of historical flowering dates documented by herbarium specimens.

    Results

    Within each species, we found a strong relationship between flowering date and latitude, such that southern populations flower earlier than northern ones. In areas of sympatry, the species flower in sequence rather than simultaneously, with flowering dates offset by ≥9 d for all species pairs. In two cases it appears that the offset in flowering times is an incidental consequence of adaptation to differing climates, but in the recently diverged sister speciesV. prunifoliumandV. rufidulum, we find evidence that reinforcement led to reproductive character displacement. Long‐term trends suggest that the two northern‐most species are flowering earlier in response to recent climate change.

    Conclusions

    We argue that speciation in theLentagoclade has primarily occurred through ecological divergence of allopatric populations, but differences in flowering time were essential to maintain separation of incipient species when they came into secondary contact. This combination of factors may underlie diversification in many other plant clades.

     
    more » « less
  4. Abstract

    Giant clams (subfamily: Tridacninae) are an important food and economic resource for the Republic of Palau and the greater Indo‐Pacific region. However, giant clam diversity and distribution data for Palau are out of date.

    This study reports the species diversity and distribution of giant clams across the Palauan archipelago (total survey area of 3,3002m) from data collected between 2015–2017.

    This is the first documented finding ofTridacna noaein Palau, however, it was rare. Only four individuals were found at only two locations.

    Results show that Palau is home to a diverse and abundant population of giant clams.Tridacna crocea(an important food and economic resource) exhibited the highest abundance, with an average of 20.0 ± 2.9 individuals per 50 m2.Tridacna maximaandTridacna squamosawere ranked next in abundance. In contrast,T. noae,Tridacna derasa,Tridacna gigas, andHippopus hippopuswere found in low numbers or only found in few locations.

    The density of all recruits, juveniles, and adultT. croceaandT. maximadid not differ significantly between conservation areas and open fishing sites, which suggests the possibility that ecological factors such as habitat loss, acute weather events, or changes in sea surface temperatures could be impacting replenishment or recruitment. However, one protected area was found to have a higher abundance ofT. crocearecruits and adults, which suggests that protection from fishing may have increased recruitment rates and lowered mortality rates at this site.

    Taken as a whole, clam populations in Palau remain reasonably abundant and healthy. As demand for giant clams continues to rise in Palau and the region, local regulations should focus on sustainable fishing practices by establishing size limits, species bans, and long‐term monitoring plans to maintain the diverse populations of giant clams found there.

     
    more » « less
  5. Synopsis

    By linking anatomical structure to mechanical performance we can improve our understanding of how selection shapes morphology. Here we examined the functional morphology of feeding in fishes of the subfamily Danioninae (order Cypriniformes) to determine aspects of cranial evolution connected with their trophic diversification. The Danioninae comprise three major lineages and each employs a different feeding strategy. We gathered data on skull form and function from species in each clade, then assessed their evolutionary dynamics using phylogenetic-comparative methods. Differences between clades are strongly associated with differences in jaw protrusion. The paedomorphic Danionella clade does not use jaw protrusion at all, members of the Danio clade use jaw protrusion for suction production and prey capture, and members of the sister clade to Danio (e.g., Devario and Microdevario) use jaw protrusion to retain prey after capture. The shape of the premaxillary bone is a major determinant of protrusion ability, and premaxilla morphology in each of these lineages is consistent with their protrusion strategies. Premaxilla shapes have evolved rapidly, which indicates that they have been subjected to strong selection. We compared premaxilla development in giant danio (Devario aequipinnatus) and zebrafish (Danio rerio) and discuss a developmental mechanism that could shift danionine fishes between the feeding strategies employed by these species and their respective clades. We also identified a highly integrated evolutionary module that has been an important factor in the evolution of trophic mechanics within the Danioninae.

     
    more » « less