Biology subjects

Camacho, J. P. M.

Publications and source records attributed to Camacho, J. P. M..

4 recordsLinked to original sources

bioRxiv2021

On the contingent nature of satellite DNA evolution

BackgroundThe full catalogue of satellite DNA (satDNA) within a same genome constitutes the satellitome. The Library Hypothesis predicts that satDNA in relative species reflects that in their common ancestor, but the evolutionary mechanisms and pathways of satDNA evolution have never been analyzed for full satellitomes. We compare here the satellitomes of two Oedipodine grasshoppers (Locusta migratoria and Oedaleus decorus) which shared their most recent common ancestor about 22.8 Ma ago. ResultsWe found that about one-third of their satDNA families (near 60 in every species) showed sequence homology and were grouped into 12 orthologous superfamilies. The turnover rate of consensus sequences was extremely variable among the 20 orthologous family pairs analyzed in both species. The satDNAs shared by both species showed poor association with sequence signatures and motives frequently argued as functional, except for short inverted repeats allowing short dyad symmetries and non-B DNA conformations. Orthologous satDNAs frequently showed different FISH patterns at both intra- and interspecific levels. We defined indices of homogenization and degeneration and quantified the level of incomplete library sorting between species. ConclusionsOur analyses revealed that satDNA degenerates through point mutation and homogenizes through partial turnovers caused by massive tandem duplications (the so-called satDNA amplification). Remarkably, satDNA amplification increases homogenization, at intragenomic level, and diversification between species, thus constituting the basis for concerted evolution. We suggest a model of satDNA evolution by means of recursive cycles of amplification and degeneration, leading to mostly contingent evolutionary pathways where concerted evolution emerges promptly after lineages split.

genomics↗

bioRxiv2021

Occasional paternal inheritance of the germline-restricted chromosome in songbirds

All songbirds have one special accessory chromosome1-4, the so-called germline-restricted chromosome (GRC)4-7, which is only present in germline cells and absent from all somatic tissues. Earlier work on the zebra finch (Taeniopygia guttata castanotis) showed that the GRC is inherited only through the female line4,6,8,9 - like mitochondrial DNA7,9-12 - and is eliminated from the sperm during spermatogenesis5,7,9-11. Here we show that the GRC can also be paternally inherited. Confocal microscopy using GRC-specific FISH probes indicated that a considerable fraction of sperm heads (1-19%) in zebra finch ejaculates still contained the GRC. In line with these cytogenetic data, sequencing of ejaculates revealed that individual males from two families differed strongly and consistently in the number of GRCs in their ejaculates. Examining a captive-bred population of hybrids of the two zebra finch subspecies (T. g. guttata and T. g. castanotis) revealed that the descendants inherited their mitochondria from a castanotis mother but their GRC from a guttata father. Moreover, GRC haplotypes across nine different castanotis matrilines showed at best a weak tendency to be co-inherited with mtDNA haplotypes. Within castanotis, the GRC showed little variability, while the mtDNA of matrilines was highly divergent. This suggests that a single GRC haplotype has recently spread across the entire castanotis population, crossing the matriline boundaries via paternal spillover. Our findings raise the possibility that certain GRC haplotypes could selfishly spread through the population, via additional paternal transmission, thereby outcompeting other GRC haplotypes that were limited to strict maternal inheritance, even if this was partly detrimental to organismal fitness.

genomics↗

bioRxiv2019

Evolutionary success of a parasitic B chromosome rests on gene content

Supernumerary (B) chromosomes are dispensable genomic elements found in most kinds of eukaryotic genomes. Many show drive mechanisms that give them an advantage in transmission, but how they achieve it remains a mystery. The recent finding of protein-coding genes in B chromosomes has opened the possibility that their evolutionary success is based on their genetic content. Using a protocol based on mapping genomic DNA Illumina reads from B-carrying and B-lacking individuals on the coding sequences of de novo transcriptomes from the same individuals, we identified 25 protein-coding genes in the B chromosome of the migratory locust, 15 of which showed a full coding region. Remarkably, one of these genes (apc1) codes for the large subunit of the Anaphase Promoting Complex or Cyclosome (APC/C), an E3 ubiquitin ligase involved in the metaphase-anaphase transition. Sequence comparison of A and B chromosome gene paralogs showed that the latter show B-specific nucleotide changes, neither of which putatively impairs protein function. These nucleotide signatures allowed identifying B-derived transcripts in B-carrying transcriptomes, and demonstrated that they show about similar frequency as A-derived ones. Since B-carrying individuals show higher amounts of apc1 transcripts than B-lacking ones, the putatively higher amount of APC1 protein might induce a faster metaphase-anaphase transition in spite of orientation of the two B chromosome chromatids towards the same pole during metaphase, thus facilitating B chromosome non-disjunction. Therefore, apc1 is the first protein-coding gene uncovered in a B chromosome that might be responsible for B chromosome drive.\n\nSignificance StatementThe genome of the migratory locust harbors a parasitic chromosome that arose about 2 million years ago. It is widespread in natural populations from Asia, Africa, Australia and Europe, i.e. all continents where this species lives. The secret for such an extraordinary evolutionary success is unveiled in this report, as B chromosomes in this species contain active protein-coding genes whose transcripts might interfere with gene expression in the host genome (the A chromosomes), thus facilitating B chromosome mitotic and meiotic drive to provide the transmission advantage which grants its success. One of the B-chromosomal genes (apc1) codes for the large subunit of the Anaphase Promoting Complex or Cyclosome (APC/C) whose expression might provide a mechanistic explanation for B chromosome drive.

evolutionary biology↗

bioRxiv2018

Programmed DNA elimination of germline development genes in songbirds

Genomes can vary within individual organisms. Programmed DNA elimination leads to dramatic changes in genome organisation during the germline-soma differentiation of ciliates1, lampreys2, nematodes3,4, and various other eukaryotes5. A particularly remarkable example of tissue-specific genome differentiation is the germline-restricted chromosome (GRC) in the zebra finch which is consistently absent from somatic cells6. Although the zebra finch is an important animal model system7, molecular evidence from its large GRC (>150 megabases) is limited to a short intergenic region8 and a single mRNA9. Here, we combined cytogenetic, genomic, transcriptomic, and proteomic evidence to resolve the evolutionary origin and functional significance of the GRC. First, by generating tissue-specific de-novo linked-read genome assemblies and re-sequencing two additional germline and soma samples, we found that the GRC contains at least 115 genes which are paralogous to single-copy genes on 18 autosomes and the Z chromosome. We detected an amplification of [≥]38 GRC-linked genes into high copy numbers (up to 308 copies) but, surprisingly, no enrichment of transposable elements on the GRC. Second, transcriptome and proteome data provided evidence for functional expression of GRC genes at the RNA and protein levels in testes and ovaries. Interestingly, the GRC is enriched for genes with highly expressed orthologs in chicken gonads and gene ontologies involved in female gonad development. Third, we detected evolutionary strata of GRC-linked genes. Developmental genes such as bicc1 and trim71 have resided on the GRC for tens of millions of years, whereas dozens have become GRC-linked very recently. The GRC is thus likely widespread in songbirds (half of all bird species) and its rapid evolution may have contributed to their diversification. Together, our results demonstrate a highly dynamic evolutionary history of the songbird GRC leading to dramatic germline-soma genome differences as a novel mechanism to minimise genetic conflict between germline and soma.

evolutionary biology↗