The Diversification and Evolution of Marine Invertebrates in Oceanic Islands

The Diversification and Evolution of Marine Invertebrates in Oceanic Islands

The Diversification and Evolution of Marine Invertebrates in Oceanic Islands

Unravelling long-established divergence patterns and remarkable geographic segregation that has endured over millions of years in marine invertebrates.

Macaronesian rocky shores.
PHOTO CREDIT: Pedro Vieira, Mafalda Tavares, Henrique Queiroga

Oceanic islands constitute prime evolutionary grounds for terrestrial organisms, promoting extensive isolation and harboring exceptional levels of diversity and endemism. Marine organisms, on the contrary, are not expected to experience evolutionary forces with the same intensity and, therefore, their diversification and evolution in oceanic landscapes has been somewhat disregarded.

Shore-dwelling marine benthic invertebrates are unique relative to both terrestrial organisms and other marine taxa. Most shore species have planktonic larvae that facilitate dispersal over open water. However, some small invertebrates, such as free-living peracarids (Peracarida: Crustacea), are more prone to isolation due to life histories characterized by direct development and putatively reduced vagility.

As a result of a DNA barcode-based screening of the diversity of littoral peracarids along Macaronesia and nearby continental shores, we have found an exceptional amount of cryptic diversity, together with a very structured geographic assortment within multiple morphospecies. We investigated, with particular detail, two common and distinct peracarid taxa present in the Macaronesian archipelagos of Azores, Madeira, and Canaries, namely 3 morphospecies of the isopod genus Dynamene1 and 7 morphospecies of the amphipod family Hyalidae2. We unraveled an additional 34 suspected new species (75% endemic of Macaronesia) with no apparent discriminative morphological features, including the noteworthy cases of the isopod Dynamene edwardsi and the amphipod Apohyale stebbingi comprising 9 and 13 putative species, respectively.

Adding to this surprising cryptic diversity, lineages within each morphospecies were also frequently exclusive to one island (50%), despite the general geographic proximity of the islands within each archipelago (e.g., from as little as 50 km between Porto Santo and Madeira). Globally, the genetic divergences among lineages within a morphospecies were also comparatively high (e.g., D. edwardsi up to 22% and A. stebbingi up to 21%), indicating a very deep evolutionary history in the region which pre-dates the Pleistocene glacial cycles (D. edwardsi lineages probably started diverging between 20 and 30 MYA).

 

Representative study species; not to scale.
PHOTO CREDIT: Pedro Vieira

There were several noteworthy findings in these studies. First, the unexpectedly high amount of diversity and endemism in these Macaronesian marine invertebrates, even within the same archipelago. Although peracarids can be assumed to have comparatively low vagility, since they lack a planktonic larval stage, there is extensive evidence for their dispersal capability and population connectivity. Namely, both our and other authors’ studies report peracarid morphospecies displaying little genetic structure over wide geographic ranges, for example, along the European continental Atlantic coasts.

Second, we were surprised to find marked geographic segregation among the newly found species. They were frequently restricted to a single island where they constituted the only representative of the cryptic complex. To a certain extent, the geographical segregation of these peracarids more closely resemble what would be expected for terrestrial organisms than marine invertebrates.

 

A. Sampling locations for each Dynamene species. B. Reduced median network of COI data from the genus Dynamene. Size of the circles are proportional to the number of similar haplotypes. Number of mutations separating each haplotype and inferred ancestors (median vectors) are displayed in black. Links displaying a single mutation do not display the number.

PHOTO CREDIT: Pedro Vieira

Finally, the combined evidence on diversity, geographic segregation, and divergence times, unraveled long-established divergence patterns and a remarkable geographic segregation that endured over millions of years till present. Therefore, the current distribution patterns of many of these peracarids cannot be elucidated through common accounts of marine invertebrates in the north-eastern Atlantic, namely processes involving dispersal, geographic proximity or Pleistocene glacial cycles. We propose alternative mechanisms for the speciation of these invertebrates in Macaronesia, such as those involving priority effects and pre-emptive exclusion, which have been seldom evoked to explain the deep segregation in the open ocean.

In the near future, we intend to investigate the genetic variability of taxa with planktonic larvae from these oceanic islands to verify if the long-term segregation patterns are exclusive of peracarid crustaceans or, instead, are more widespread patterns in marine invertebrates in Macaronesia.

References

  1. Vieira PE, Desiderato A, Holdich DM, Soares P, Creer S, Carvalho GR, Costa FO, Queiroga H (2019) Deep segregation in the open ocean: Macaronesia as an evolutionary hotspot for low dispersal marine invertebrates. Molecular Ecology. https://doi.org/10.1111/mec.15052
  2. Desiderato A, Costa FO, Serejo CS, Abbiati M, Queiroga H, Vieira PE (2019) Macaronesian islands as promoters of diversification in amphipods: The remarkable case of the family Hyalidae (Crustacea, Amphipoda). Zoologica Scripta. https://doi.org/10.1111/zsc.12339

Written by

Pedro Vieira

Pedro Vieira

University of Minho, Braga, Portugal

Filipe Costa

Filipe Costa

University of Minho, Braga, Portugal

April 7, 2019
PDF
https://doi.org/10.21083/ibol.v9i1.5477

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DNA Barcoding and Genomics in the Megadiverse Amazon Altitude Fields

DNA Barcoding and Genomics in the Megadiverse Amazon Altitude Fields

DNA BARCODING AND GENOMICS IN THE MEGADIVERSE AMAZON ALTITUDE FIELDS

Scientists are contributing to the most profound molecular representation of biodiversity in any Brazilian environment.

The entrance of a ferruginous cave at the Bocaina mountain in the Carajás region, Pará State, Brazil.

PHOTO CREDIT: João Marcos Rosa.

Industrial activities in the Brazilian Amazon are highly regulated by governmental agencies. However, the lack of knowledge about megadiverse areas is a problem for the establishment of best conservation practices; this is the case for mining operations in the eastern Amazonian Carajás, a region comprised of a mosaic of national parks, indigenous peoples’ conservation areas, and nature reserves. Of particular interest are the ferruginous altitude fields known as the Canga. Our floristic survey described the presence of 1,094 species from just over 200 previously known1. The lack of biodiversity data is even more significant for the ferruginous caves where only around 10 invertebrate species are identified to the species level. Unfortunately, this is typical for the Amazon basin.

To provide reliable scientific data that contributes to the implementation of best conservation practices, Instituto Tecnológico Vale is developing DNA barcode reference libraries for the flora, cave invertebrates, and bats of the region, and providing deeper genomic references for species that are endangered or difficult to identify. To achieve this goal, we established the necessary infrastructure to conduct DNA sequencing using Sanger, Illumina, and PacBio technologies, coupled with high-performance computing, artificial intelligence algorithms, and highly trained personnel.

 

Botanists collecting samples in a temporary lake in ferruginous altitude fields in the Carajás region, Pará State, Brazil.
PHOTO CREDIT: João Marcos Rosa

To date, over 8,575 barcodes for 3,548 specimens of plants and invertebrates have been produced, while a large number of species remain to be identified by morphological attributes. Morphological specimen determination is conducted by in-house specialists, as well as by an extensive network of specialists in universities and museums across Brazil and abroad.

For this purpose, nuclear and chloroplast or mitochondrial markers as well as low coverage to whole genome sequencing or restriction site-associated DNA sequencing (RADSeq) are being employed to unravel the vast genetic diversity of the biota of Carajás2-4. For several endemic plants, such as species of Asteraceae, Melastomataceae5, Convolvulaceae6, and Isoetaceae2, diversity analyses, based on next-generation sequencing, aim to characterize the genetic variability among and within populations, as well as the identification of markers under selective pressure. These methods also contribute to the understanding of population structure and the process of gene flow between populations affected by natural factors and industrial operations. Models of environmental distribution, including parameters sensitive to climate change, were determined for several taxonomic groups, including plants and bats7.

Specimens of the pinheirinho-da-canga (Paepalanthus fasciculoides) highly adapted to inhabit the canga (ancient ferruginous rock outcrops) at the altitude fields in the Carajás region, Pará State, Brazil.
PHOTO CREDIT: João Marcos Rosa
We are also establishing eDNA methods, as well as metagenomics and metaproteomics data for environmental monitoring of ferruginous fields phytophysiognomies, areas under rehabilitation processes, and caves8. Together these data constitute the most profound molecular representation of any environment in Brazil. We have contributed a total of 3,072 specimens to the Barcode of Life Data System (BOLD) comprising 398 genera (291 new) in addition to the 408 different genera collected through the national effort for angiosperms in Brazil. We have also provided 571 cave fauna specimens.

It is important to highlight that all of these data generated are being provided to the public and its use will be critical to the conservation of such a unique collection of species.

References:

1. Brazil Flora Group (2018) Growing knowledge: an overview of Seed Plant diversity in Brazil. Rodriguésia 66(4): 1085–1113. http://dx.doi.org/10.1590/2175-7860201566411

2. Nunes GL, Oliveira RRM, Guimarães JTF, Giulietti AM, Caldeira C, Vasconcelos S, et al., (2018) Quillworts from the Amazon: A multidisciplinary populational study on Isoetes serracarajensis and Isoetes cangae. PLoS ONE 13(8): e0201417. https://doi.org/10.1371/journal.pone.0201417

3. Ramalho AJ, Zappi DC, Nunes GL, Watanabe MTC, Vasconcelos S, Dias MC, Jaffé R, Prous X, Giannini TC, Oliveira G and Giulietti AM (2018) Blind testing: DNA barcoding sheds light upon the identity of plant fragments as a subsidy for cave conservation. Frontiers in Plant Science 9:1052. https://doi.org/10.3389/fpls.2018.01052

4. Oliveira RRMO, Vasconcelos S, Pires ES, Pietrobon T, Prous X and Oliveira G (2019) Complete mitochondrial genomes of three troglophile cave spiders (Mesabolivar, pholcidae), Mitochondrial DNA Part B 4(1): 251–252. https://doi.org/10.1080/23802359.2018.1547139

5. Carvalho CdS, Lanes ECM, Silva AR, Caldeira CF, Carvalho-Filho N, Gastauer M, Imperatriz-Fonseca VL, Nascimento W, Oliveira G, Siqueira JO, Viana PL, Jaffe R (2019) Habitat loss does not always entail negative genetic consequences. bioRxiv 528430. https://doi.org/10.1101/528430

6. Lanes ÉC, Pope NS, Alves R, Carvalho Filho NM, Giannini TC, Giulietti AM, Imperatriz-Fonseca VL, Monteiro W, Oliveira G, Silva AR, Siqueira JO, Souza-Filho PW, Vasconcelos S and Jaffé R (2018) Landscape genomic conservation assessment of a narrow-endemic and a widespread morning glory from Amazonian Savannas. Frontiers in Plant Science 9:532. https://doi.org/10.3389/fpls.2018.00532

7. Costa WF, Ribeiro M, Saraiva AM, Imperatriz-Fonseca VL, Giannini TC (2018) Bat diversity in Carajás National Forest (Eastern Amazon) and potential impacts on ecosystem services under climate change. Biological Conservation 218: 200–210. https://doi.org/10.1016/j.biocon.2017.12.034

8. Gastauer M, Vero MPO, de Souza KP, Pires ES, Alves R, Caldeira CF, Ramos SJ, Oliveira G (2019) A metagenomic survey of soil microbial communities along a rehabilitation chronosequence after iron ore mining. Scientific Data 6:190008. https://doi.org/10.1038/sdata.2019.8

Written by

Guilherme Oliveira

Guilherme Oliveira

Environmental Genomics Group, Instituto Tecnológico Vale, Belém, Brazil

Gisele Nunes Lopes

Gisele Nunes Lopes

Environmental Genomics Group, Instituto Tecnológico Vale, Belém, Brazil

Rafael Valadares

Rafael Valadares

Environmental Genomics Group, Instituto Tecnológico Vale, Belém, Brazil

Ronnie Alves

Ronnie Alves

Environmental Genomics Group, Instituto Tecnológico Vale, Belém, Brazil

Santelmo Vasconcelos

Santelmo Vasconcelos

Environmental Genomics Group, Instituto Tecnológico Vale, Belém, Brazil

April 7, 2019
PDF
https://doi.org/10.21083/ibol.v9i1.5498

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