Alexander Hayward

The phylogeographical clade trade: tracing the impact of human-mediated dispersal on the colonization of northern Europe by the oak gallwasp Andricus kollari.

Human dispersal of organisms is an important process modifying natural patterns of biodiversity. Such dispersal generates new patterns of genetic diversity that overlie natural phylogeographical signatures, allowing discrimination between alternative dispersal mechanisms. Here we use allele frequency and DNA sequence data to distinguish between alternative scenarios (unassisted range expansion and long range introduction) for the colonization of northern Europe by an oak‐feeding gallwasp, Andricus kollari. Native to Mediterranean latitudes from Portugal to Iran, this species became established in northern Europe following human introduction of a host plant, the Turkey oak Quercus cerris. Colonization of northern Europe is possible through three alternative routes: (i) unassisted range expansion from natural populations in the Iberian Peninsula; (ii) unassisted range expansion from natural populations in Italy and Hungary; or (iii) descent from populations imported to the UK as trade goods from the eastern Mediterranean in the 1830s. We show that while populations in France were colonized from sources in Italy and Hungary, populations in the UK and neighbouring parts of coastal northern Europe encompass allozyme and sequence variation absent from the known native range. Further, these populations show demographic signatures expected for large stable populations, rather than signatures of rapid population growth from small numbers of founders. The extent and spatial distribution of genetic diversity in the UK suggests that these A. kollari populations are derived from introductions of large numbers of individuals from each of two genetically divergent centres of diversity in the eastern Mediterranean. The strong spatial patterning in genetic diversity observed between different regions of northern Europe, and between sites in the UK, is compatible with leptokurtic models of population establishment.

Comparative phylogeography across two trophic levels: the oak gall wasp Andricus kollari and its chalcid parasitoid Megastigmus stigmatizans

Insect parasitoids are important components of many terrestrial ecosystems. However, relatively little is known about the mechanisms responsible for structuring their populations. Here we investigate the ability of Megastigmus stigmatizans, an oak gall wasp parasitoid, to track its host Andricus kollari over two different timescales, and examine its current population structure across a divide in host population structure. The divide represents a transition in gall wasp host‐plant species and offers the opportunity to examine whether the split, which divides gall wasp populations, manifests itself in the next trophic level. Analysis of mitochondrial haplotype data for parasitoid and host reveals: (i) A similar phylogeographic population structure for both, with Iberian populations more derived with respect to more eastern populations. (ii) It is likely that the host colonized the Iberian refuge earlier than the parasitoid, probably by at least one glacial cycle. (iii) Recent range expansion of central European host populations northwards has resulted in pursuit by parasitoids from the same geographic origin. (iv) In addition, Iberian parasitoid populations have crossed a major divide in host population structure to invade northern Europe. Such human‐facilitated escape from natural refugial distributions may have important implications for the composition and structure of northern European gall wasp communities.

Concordant phylogeography and cryptic speciation in two Western Palaearctic oak gall parasitoid species complexes

Little is known about the evolutionary history of most complex multi‐trophic insect communities. Widespread species from different trophic levels might evolve in parallel, showing similar spatial patterns and either congruent temporal patterns (Contemporary Host‐tracking) or later divergence in higher trophic levels (Delayed Host‐tracking). Alternatively, host shifts by natural enemies among communities centred on different host resources could disrupt any common community phylogeographic pattern. We examined these alternative models using two Megastigmus parasitoid morphospecies associated with oak cynipid galls sampled throughout their Western Palaearctic distributions. Based on existing host cynipid data, a parallel evolution model predicts that eastern regions of the Western Palaearctic should contain ancestral populations with range expansions across Europe about 1.6 million years ago and deeper species‐level divergence at both 8–9 and 4–5 million years ago. Sequence data from mitochondrial cytochrome b and multiple nuclear genes showed similar phylogenetic patterns and revealed cryptic genetic species within both morphospecies, indicating greater diversity in these communities than previously thought. Phylogeographic divergence was apparent in most cryptic species between relatively stable, diverse, putatively ancestral populations in Asia Minor and the Middle East, and genetically depauperate, rapidly expanding populations in Europe, paralleling patterns in host gallwasp species. Mitochondrial and nuclear data also suggested that Europe may have been colonized multiple times from eastern source populations since the late Miocene. Temporal patterns of lineage divergence were congruent within and across trophic levels, supporting the Contemporary Host‐tracking Hypothesis for community evolution.

Pan-vertebrate comparative genomics unmasks retrovirus macroevolution

Significance For millions of years retroviruses, such as HIV in humans, have attacked vertebrates. Occasionally retroviruses infiltrate germ cells, incorporate themselves into the host’s genome, and transmit vertically to the host’s offspring as endogenous retroviruses (ERVs). Consequently, ERVs make up large portions of vertebrate genomes and represent a record of past host–retrovirus interactions. We developed pan-vertebrate ERV analyses to provide an overview of host–retrovirus interactions, generating insights into retroviral evolution, diversity, host-switching, and the factors influencing retroviral transmission. Astoundingly, we found over 36,000 ERV lineages across our sample of vertebrate diversity. The results provide knowledge about host–retrovirus coevolution, suggesting an unprecedented ability of retroviruses to switch between distantly related vertebrates and implying existence of additional, yet unidentified retroviruses. Although extensive research has demonstrated host-retrovirus microevolutionary dynamics, it has been difficult to gain a deeper understanding of the macroevolutionary patterns of host–retrovirus interactions. Here we use recent technological advances to infer broad patterns in retroviral diversity, evolution, and host–virus relationships by using a large-scale phylogenomic approach using endogenous retroviruses (ERVs). Retroviruses insert a proviral DNA copy into the host cell genome to produce new viruses. ERVs are provirus insertions in germline cells that are inherited down the host lineage and consequently present a record of past host–viral associations. By mining ERVs from 65 host genomes sampled across vertebrate diversity, we uncover a great diversity of ERVs, indicating that retroviral sequences are much more prevalent and widespread across vertebrates than previously appreciated. The majority of ERV clades that we recover do not contain known retroviruses, implying either that retroviral lineages are highly transient over evolutionary time or that a considerable number of retroviruses remain to be identified. By characterizing the distribution of ERVs, we show that no major vertebrate lineage has escaped retroviral activity and that retroviruses are extreme host generalists, having an unprecedented ability for rampant host switching among distantly related vertebrates. In addition, we examine whether the distribution of ERVs can be explained by host factors predicted to influence viral transmission and find that internal fertilization has a pronounced effect on retroviral colonization of host genomes. By capturing the mode and pattern of retroviral evolution and contrasting ERV diversity with known retroviral diversity, our study provides a cohesive framework to understand host–virus coevolution better.

Comparative genomic and phylogenetic analysis of vitellogenin and other large lipid transfer proteins in metazoans

Vitellogenins and other large lipid transfer proteins (LLTP) are well known to play significant roles in the development, metabolism and reproduction of animals. Comparative genomics and phylogenetic analyses of LLTPs using the most comprehensive dataset in metazoans to date are carried out. Our analyses demonstrate that LLTP genes arose significantly earlier, and are more widespread than previously proposed – being present in numerous additional bilaterian and non‐bilaterian lineages. A hypothesis is advanced that the most ancestral animal LLTP gene is Vtg, while loss of domains occurred at the bilaterians stem giving rise to apolipoprotein and microsomal triglyceride transfer proteins genes.

Comparative support for the expensive tissue hypothesis: Big brains are correlated with smaller gut and greater parental investment in Lake Tanganyika cichlids

The brain is one of the most energetically expensive organs in the vertebrate body. Consequently, the energetic requirements of encephalization are suggested to impose considerable constraints on brain size evolution. Three main hypotheses concerning how energetic constraints might affect brain evolution predict covariation between brain investment and (1) investment into other costly tissues, (2) overall metabolic rate, and (3) reproductive investment. To date, these hypotheses have mainly been tested in homeothermic animals and the existing data are inconclusive. However, there are good reasons to believe that energetic limitations might play a role in large‐scale patterns of brain size evolution also in ectothermic vertebrates. Here, we test these hypotheses in a group of ectothermic vertebrates, the Lake Tanganyika cichlid fishes. After controlling for the effect of shared ancestry and confounding ecological variables, we find a negative association between brain size and gut size. Furthermore, we find that the evolution of a larger brain is accompanied by increased reproductive investment into egg size and parental care. Our results indicate that the energetic costs of encephalization may be an important general factor involved in the evolution of brain size also in ectothermic vertebrates.

Phylogeny and DNA barcoding of inquiline oak gallwasps (Hymenoptera: Cynipidae) of the Western Palaearctic.

We examine phylogenetic relationships within the Synergus complex of herbivorous inquiline gallwasps (Hymenoptera; Cynipidae; Synergini) associated with cynipid host galls on oak, a biologically diverse group whose genus-level morphological taxonomy has long been considered stable but whose species level taxonomy is problematic. We incorporate data for over 70% of recognised Western Palaearctic species in five morphology-based genera (Ceroptres, Saphonecrus, Synergus, Synophrus, Ufo), comprising sequence for two mitochondrial loci (coxI, cytb) and one nuclear locus (28S D2). In particular, we assess the evidence for monophyly of two long-established, morphology-defined sections within the genus Synergus that differ in a range of biological traits. To aid analyses of ecological interactions within oak cynipid communities, we also consider the utility of cytochrome oxidase I (coxI) DNA barcodes in the oak inquilines. In this assessment, we do not assume that species are delineated at a single threshold value of sequence divergence for a single gene, but examine concordance in the composition of molecular operational Taxonomic units (MOTUs) across a range of sequence divergences in each gene and across genes. We also assess the impact of sampling effort on MOTU stability. Phylogenetic reconstructions for all three loci support monophyly for Synergus and Synophrus, but reject monophyly for Saphonecrus and for the two sections within Synergus. The suites of traits associated with the two sections of the genus Synergus are thus homoplasious. All three loci also reject monophyly for three Synergus species (S. hayneanus, S. pallipes, S. umbraculus). Sequences for each locus identify robust MOTUs that are largely concordant across loci for a range of cut-off values. Though many MOTUs correspond to recognised Linnean species, there is significant, multigene disagreement between groupings supported by morphology and sequence data, with both allocation of different morphospecies to the same MOTU and allocation of the same morphospecies to multiple MOTUs, regardless of cut-off value. Our results imply that while DNA barcoding has considerable utility within this group, morphology-based identification needs major revision at both genus and species levels. Further, lifehistory traits currently attributed to single morphospecies probably confound attributes of multiple lineages. Revealing patterns of character state evolution in Synergus requires collection of new host association and life history data explicitly linked to DNA barcode data for the specimens concerned.

Comparative support for the expensivetissue hypothesis: Big brains are correlatedwith smaller gut and greater parentalinvestment in Lake Tanganyika cichlids

The brain is one of the most energetically expensive organs in the vertebrate body. Consequently, the energetic requirements of encephalization are suggested to impose considerable constraints on brain size evolution. Three main hypotheses concerning how energetic constraints might affect brain evolution predict covariation between brain investment and (1) investment into other costly tissues, (2) overall metabolic rate, and (3) reproductive investment. To date, these hypotheses have mainly been tested in homeothermic animals and the existing data are inconclusive. However, there are good reasons to believe that energetic limitations might play a role in large‐scale patterns of brain size evolution also in ectothermic vertebrates. Here, we test these hypotheses in a group of ectothermic vertebrates, the Lake Tanganyika cichlid fishes. After controlling for the effect of shared ancestry and confounding ecological variables, we find a negative association between brain size and gut size. Furthermore, we find that the evolution of a larger brain is accompanied by increased reproductive investment into egg size and parental care. Our results indicate that the energetic costs of encephalization may be an important general factor involved in the evolution of brain size also in ectothermic vertebrates.

Broad-scale phylogenomics provides insights into retrovirus–host evolution

Significance Retroviruses, such as HIV, are important pathogens of vertebrates, including humans. They are capable of crossing species barriers to infect new hosts, but knowledge about the evolutionary history of retroviruses is limited. However, genomic traces of past retrovirus activities known as “endogenous retroviruses” can be screened from sequenced genomes and analyzed to improve understanding of retrovirus evolution. Here we use a unique approach to address the evolution of one group of retroviruses in a screen of 60 diverse vertebrate host genomes. We find evidence of rampant host-switching across mammalian orders by members of this group throughout their evolutionary history. We also find evidence that the spread of infective retroviruses from this group may be facilitated by rats. Genomic data provide an excellent resource to improve understanding of retrovirus evolution and the complex relationships among viruses and their hosts. In conjunction with broad-scale in silico screening of vertebrate genomes, this resource offers an opportunity to complement data on the evolution and frequency of past retroviral spread and so evaluate future risks and limitations for horizontal transmission between different host species. Here, we develop a methodology for extracting phylogenetic signal from large endogenous retrovirus (ERV) datasets by collapsing information to facilitate broad-scale phylogenomics across a wide sample of hosts. Starting with nearly 90,000 ERVs from 60 vertebrate host genomes, we construct phylogenetic hypotheses and draw inferences regarding the designation, host distribution, origin, and transmission of the Gammaretrovirus genus and associated class I ERVs. Our results uncover remarkable depths in retroviral sequence diversity, supported within a phylogenetic context. This finding suggests that current infectious exogenous retrovirus diversity may be underestimated, adding credence to the possibility that many additional exogenous retroviruses may remain to be discovered in vertebrate taxa. We demonstrate a history of frequent horizontal interorder transmissions from a rodent reservoir and suggest that rats may have acted as important overlooked facilitators of gammaretrovirus spread across diverse mammalian hosts. Together, these results demonstrate the promise of the methodology used here to analyze large ERV datasets and improve understanding of retroviral evolution and diversity for utilization in wider applications.

Evolution and functional divergence of enzymes involved in sesquiterpenoid hormone biosynthesis in crustaceans and insects.

Juvenile hormone (JH) and methyl farnesoate (MF) play well-known roles in the development and reproduction of insects and crustaceans. Juvenile hormone acid O-methyltransferase (JHAMT) and farnesoic acid O-methyltransferase (FAMeT) are the enzymes responsible for catalyzing the biosynthesis of JH and MF, respectively. It is not clear whether the genes that encode these enzymes are present in animal lineages outside of the arthropods. Based on DNA sequence similarity, the literature suggests that an FAMeT ortholog is present in humans. However, vertebrates do not appear to produce JH or MF. To help unravel the evolution of hormonal systems in animals we have carried out the first comparative genomic analysis of JHAMT and FAMeT. We identify the first JHAMT ortholog in a crustacean genome, and FAMeT orthologs in annelid and cephalochordate genomes. Moreover, phylogenetic analyses suggest that there is no true homolog of FAMeT in humans contrary to previous hypotheses. Our analyses suggest that the presence of multiple FAMeT isoforms in arthropods may be a consequence of different evolutionary mechanisms. The genes responsible for hormone biosynthesis in extant insects and crustaceans appear to have been present at least in the Pancrustacea. Different selective forces appear to have subsequently acted on the two lineages, leading to the present functional divergence. Our use of comparative genomics and phylogenetic analysis advance knowledge of the relationships of the hormonal enzyme genes in question, and provide new insights into the evolution of hormonal systems in the largest animal phylum, the Arthropoda.