Stacy A. Krueger-Hadfield

Invasion of novel habitats uncouples haplo-diplontic life cycles

Bakers Law predicts uniparental reproduction will facilitate colonization success in novel habitats. While evidence supports this prediction among colonizing plants and animals, few studies have investigated shifts in reproductive mode in haplo‐diplontic species in which both prolonged haploid and diploid stages separate meiosis and fertilization in time and space. Due to this separation, asexual reproduction can yield the dominance of one of the ploidy stages in colonizing populations. We tested for shifts in ploidy and reproductive mode across native and introduced populations of the red seaweed Gracilaria vermiculophylla. Native populations in the northwest Pacific Ocean were nearly always attached by holdfasts to hard substrata and, as is characteristic of the genus, haploid–diploid ratios were slightly diploid‐biased. In contrast, along North American and European coastlines, introduced populations nearly always floated atop soft‐sediment mudflats and were overwhelmingly dominated by diploid thalli without holdfasts. Introduced populations exhibited population genetic signals consistent with extensive vegetative fragmentation, while native populations did not. Thus, the ecological shift from attached to unattached thalli, ostensibly necessitated by the invasion of soft‐sediment habitats, correlated with shifts from sexual to asexual reproduction and slight to strong diploid bias. We extend Bakers Law by predicting other colonizing haplo‐diplontic species will show similar increases in asexuality that correlate with the dominance of one ploidy stage. Labile mating systems likely facilitate colonization success and subsequent range expansion, but for haplo‐diplontic species, the long‐term eco‐evolutionary impacts will depend on which ploidy stage is lost and the degree to which asexual reproduction is canalized.

Chondrus crispus – A Present and Historical Model Organism for Red Seaweeds

Abstract Chondrus crispus, or Irish moss, is a common edible red seaweed that can be found on rocky shores in the Northern Atlantic. The cell wall contains carrageenan and C. crispus is the original source of this commercially used thickener. Because of the ecological and economic importance of this red alga a relatively important research literature exists and one of the recent achievements in C. crispus research is the sequencing of its genome. In this chapter we review some of the literature with the aim to promote C. crispus as a model organism for florideophyte red seaweeds. We consider subjects like commercial and historical uses, ecology, genetics, population structure, mating systems, physiology, cell wall biology and genomics.

Development and characterization of microsatellite loci for the haploid–diploid red seaweed Gracilaria vermiculophylla

Microsatellite loci are popular molecular markers due to their resolution in distinguishing individual genotypes. However, they have rarely been used to explore the population dynamics in species with biphasic life cycles in which both haploid and diploid stages develop into independent, functional organisms. We developed microsatellite loci for the haploid–diploid red seaweed Gracilaria vermiculophylla, a widespread non-native species in coastal estuaries of the Northern hemisphere. Forty-two loci were screened for amplification and polymorphism. Nine of these loci were polymorphic across four populations of the extant range with two to eleven alleles observed. Mean observed and expected heterozygosities ranged from 0.265 to 0.527 and 0.317 to 0.387, respectively. Overall, these markers will aid in the study of the invasive history of this seaweed and further studies on the population dynamics of this important haploid–diploid primary producer.

Genetic identification of source and likely vector of a widespread marine invader

Abstract The identification of native sources and vectors of introduced species informs their ecological and evolutionary history and may guide policies that seek to prevent future introductions. Population genetics provides a powerful set of tools to identify origins and vectors. However, these tools can mislead when the native range is poorly sampled or few molecular markers are used. Here, we traced the introduction of the Asian seaweed Gracilaria vermiculophylla (Rhodophyta) into estuaries in coastal western North America, the eastern United States, Europe, and northwestern Africa by genotyping more than 2,500 thalli from 37 native and 53 non‐native sites at mitochondrial cox1 and 10 nuclear microsatellite loci. Overall, greater than 90% of introduced thalli had a genetic signature similar to thalli sampled from the coastline of northeastern Japan, strongly indicating this region served as the principal source of the invasion. Notably, northeastern Japan exported the vast majority of the oyster Crassostrea gigas during the 20th century. The preponderance of evidence suggests G. vermiculophylla may have been inadvertently introduced with C. gigas shipments and that northeastern Japan is a common source region for estuarine invaders. Each invaded coastline reflected a complex mix of direct introductions from Japan and secondary introductions from other invaded coastlines. The spread of G. vermiculophylla along each coastline was likely facilitated by aquaculture, fishing, and boating activities. Our ability to document a source region was enabled by a robust sampling of locations and loci that previous studies lacked and strong phylogeographic structure along native coastlines.

Combining niche shift and population genetic analyses predicts rapid phenotypic evolution during invasion

The rapid evolution of non‐native species can facilitate invasion success, but recent reviews indicate that such microevolution rarely yields expansion of the climatic niche in the introduced habitats. However, because some invasions originate from a geographically restricted portion of the native species range and its climatic niche, it is possible that the frequency, direction, and magnitude of phenotypic evolution during invasion have been underestimated. We explored the utility of niche shift analyses in the red seaweed Gracilaria vermiculophylla, which expanded its range from the northeastern coastline of Japan to North America, Europe, and northwestern Africa within the last 100 years. A genetically informed climatic niche shift analysis indicates that native source populations occur in colder and highly seasonal habitats, while most non‐native populations typically occur in warmer, less seasonal habitats. This climatic niche expansion predicts that non‐native populations evolved greater tolerance for elevated heat conditions relative to native source populations. We assayed 935 field‐collected and 325 common‐garden thalli from 40 locations, and as predicted, non‐native populations had greater tolerance for ecologically relevant extreme heat (40°C) than did Japanese source populations. Non‐native populations also had greater tolerance for cold and low‐salinity stresses relative to source populations. The importance of local adaptation to warm temperatures during invasion was reinforced by evolution of parallel clines: Populations from warmer, lower‐latitude estuaries had greater heat tolerance than did populations from colder, higher‐latitude estuaries in both Japan and eastern North America. We conclude that rapid evolution plays an important role in facilitating the invasion success of this and perhaps other non‐native marine species. Genetically informed ecological niche analyses readily generate clear predictions of phenotypic shifts during invasions and may help to resolve debate over the frequency of niche conservatism versus rapid adaptation during invasion.

The importance of effective sampling for exploring the population dynamics of haploid–diploid seaweeds

The mating system partitions genetic diversity within and among populations and the links between life history traits and mating systems have been extensively studied in diploid organisms. As such most evolutionary theory is focused on species for which sexual reproduction occurs between diploid male and diploid female individuals. However, there are many multicellular organisms with biphasic life cycles in which the haploid stage is prolonged and undergoes substantial somatic development. In particular, biphasic life cycles are found across green, brown and red macroalgae. Yet, few studies have addressed the population structure and genetic diversity in both the haploid and diploid stages in these life cycles. We have developed some broad guidelines with which to develop population genetic studies of haploid‐diploid macroalgae and to quantify the relationship between power and sampling strategy. We address three common goals for studying macroalgal population dynamics, including haploid‐diploid ratios, genetic structure and paternity analyses.

THE IDENTIFICATION OF SOURCE AND VECTOR OF A PROLIFIC MARINE INVADER

The source and vector of an introduced species inform its ecological and evolutionary history and may guide management that seeks to prevent future introductions. Surprisingly, few studies have successfully used genetic tools to independently inform the specific source and pathway of biological invasions. The ecological history of many introduced species, including their origins and vectors, is often based on suppositions or educated guesses. Here, we used mitochondrial and microsatellite genotyping to trace the invasion of the Asian seaweed Gracilaria vermiculophylla (Rhodophyta) along the three coastlines of the Northern Hemisphere to which it has been introduced: the western coast of North America, eastern coast of the United States and the coasts of Europe and northwest Africa. Analyzing 37 native and 53 introduced sites, we identified the Pacific coastline of northeastern Japan as the ultimate source of the Northern Hemisphere invasion. Coincidentally, most exports of the oyster Crassostrea gigas historically originated from this region and both species often grow in close proximity. Based on genetic signatures, each of the three coastlines likely received thalli directly from Japan, as well as material from another introduced coastline (i.e., a secondary invasion). Our ability to document a source region, which was enabled by a robust sampling of locations and loci that previous studies lacked, reflected strong phylogeographic structure along native coastlines. We suggest Gracilaria vermiculophylla is an important representative example of many species likely exported out of Japan by the oyster trade and its genetic signatures that may be a hallmark of oyster introduction legacies.

New Record of the non-Native Seaweed Gracilaria parvispora in Baja California - A Note on Vergara-Rodarte et al. (2016)

Abstract The delimitation of species in the Gracilariales is often difficult due to the lack of diagnostic morphological characters. As a result, non-native species are often misidentified without the use of molecular tools. Recently, studies have investigated the agar quality of the dominant gracilarioid species in the Laguna San Ignacio in Baja Califronia Sur, Mexico, including Vergara-Rodarte et al., (2016) published in the May edition of Cryptogamie, Algologie. The species has been reported as Gracilaria pacifica, G. vermiculophylla and Gracilariopsis sp. Using a combination of three mitochondrial and plastid markers, we identified this species as G. parvispora, extending the known distribution of this non-native species in Baja California. Due to the potential of G. parvispora as a source of agar, more detailed studies of on the invasion history and surveys are necessary in the eastern Pacific to determine its current distribution and impacts on the native biodiversity.

Nonnative Gracilaria vermiculophylla tetrasporophytes are more difficult to debranch and are less nutritious than gametophytes

Theory predicts that the maintenance of haplodiplontic life cycles requires ecological differences between the haploid gametophytes and diploid sporophytes, yet evidence of such differences remain scarce. The haplodiplontic red seaweed Gracilaria vermiculophylla has invaded the temperate estuaries of the Northern Hemisphere, where it commonly modifies detrital and trophic pathways. In native populations, abundant hard substratum enables spore settlement, and gametophyte:tetrasporophyte ratios are ~40:60. In contrast, many non‐native populations persist in soft‐sediment habitats without abundant hard substratum, and can be 90%–100% tetrasporophytic. To test for ecologically relevant phenotypic differences, we measured thallus morphology, protein content, organic content, “debranching resistance” (i.e., tensile force required to remove a branch from its main axis node), and material properties between male gametophytes, female gametophytes, and tetrasporophytes from a single, nonnative site in Charleston Harbor, South Carolina, USA in 2015 and 2016. Thallus length and surface area to volume ratio differed between years, but were not significantly different between ploidies. Tetrasporophytes had lower protein content than gametophytes, suggesting the latter may be more attractive to consumers. More force was required to pull a branch from the main axis of tetrasporophytes relative to gametophytes. A difference in debranching resistance may help to maintain tetrasporophyte thallus durability relative to gametophytes, providing a potential advantage in free‐floating populations. These data may shed light on the invasion ecology of an important ecosystem engineer, and may advance our understanding of life cycle evolution and the maintenance of life cycle diversity.

When Invaders Go Unnoticed: The Case of Gracilaria vermiculophylla in the British Isles

Abstract Our knowledge of non-native algae in benthic estuarine habitats is relatively poor, especially compared to algal introductions along open shores or on floating structures. Gracilaria vermiculophylla is a widespread macroalgal invader in the temperate estuaries of the Northern Hemisphere, and, here, we expand its documented range within northeastern Ireland and England. Established populations occur within two inlets in the border counties, Carlingford Lough (Counties Louth and Down) and Dundrum Bay (County Down), but G. vermiculophylla is absent from open coasts between these sites. Repeated surveys in Dundrum Bay showed variable abundances, with an increase in biomass between 2013 and 2016. Three populations were discovered in England, where this species had not previously been identified: Christchurch Harbour (Dorset), Brownsea Island in Poole Harbour (Dorset), and Kingsbridge Estuary (Devon). The Irish and English thalli belong to the most common, invasive cox1 haplotype 6. Using a combination of morphological observations and 10 microsatellite loci, we found that the population at Carlingford Lough included both reproductive haploid gametophytes and diploid tetrasporophytes and genetic signatures of sexual reproduction, but the populations at Christchurch and Brownsea displayed signatures of partial clonality. Genetic diversity was higher along the south coast of England as compared to the Irish population, consistent with patterns of diversity previously described for the European coasts. Finally, we also note the occurrence of a putative G. vermiculophylla population in Wales at Porthmadog, Gwynedd. As the sites in which we have now documented G. vermiculophylla in the British Isles also host shellfish aquaculture activities, our study is further evidence for the role of aquaculture in the spread of invasive species.