The late blooming amphipods: Global change promoted post-Jurassic ecological radiation despite Palaeozoic origin

https://doi.org/10.1016/j.ympev.2019.106664Get rights and content

Highlights

  • First fossil-based time-calibrated molecular phylogeny of Amphipoda.

  • Amphipods originated in the Palaeozoic, major clades appeared in the Late Mesozoic.

  • Ecological radiation ensued post-Jurassic, corresponding with significant global change.

  • Sequence data and morphology point towards similar systematic concepts.

Abstract

The ecological radiation of amphipods is striking among crustaceans. Despite high diversity, global distribution and key roles in all aquatic environments, little is known about their ecological transitions, evolutionary timescale and phylogenetic relationships. It has previously been proposed that the amphipod ecological diversification began in the Late Palaeozoic. By contrast, due to their affinity for cold/oxygenated water and absence of pre-Cenozoic fossils, we hypothesized that the ecological divergence of amphipods arose throughout the cool Late Mesozoic/Cenozoic. We tested our hypothesis by inferring a large-scale, time-calibrated, multilocus phylogeny, and reconstructed evolutionary patterns for major ecological traits. Although our results reveal a Late Palaeozoic amphipod origin, diversification and ecological divergence ensued only in the Late Mesozoic, overcoming a protracted stasis in marine littoral habitats. Multiple independent post-Jurassic radiations took place in deep-sea, freshwater, terrestrial, pelagic and symbiotic environments, usually postdating deep-sea faunal extinctions, and corresponding with significant climatic cooling, tectonic reconfiguration, continental flooding, and increased oceanic oxygenation. We conclude that the profound Late Mesozoic global changes triggered a tipping point in amphipod evolution by unlocking ecological opportunities that promoted radiation into many new niches. Our study also provides a solid, time-calibrated, evolutionary framework to accelerate research on this overlooked, yet globally important taxon.

Introduction

Global environmental changes shaped biodiversity patterns throughout Earth’s history (Condamine et al., 2013, Hannisdal and Peters, 2011, Roelants et al., 2007). Understanding the historical factors that triggered large-scale evolutionary radiations or extinctions remains a central tenet in evolutionary biology. Investigating the effects of these past changes at the planetary level requires suitable model systems, which can be represented by species rich taxonomic groups with a global distribution and high ecological diversity.

The Amphipoda is among the most ecologically diverse and speciose crustacean orders, encompassing over 10,000 species (Arfianti et al., 2018, Horton et al., 2019) inhabiting all aquatic environments worldwide, from hadal depths to alpine freshwater streams, from lightless groundwater to tropical forests, and from sea bottom sediments to the entrails of gelatinous plankton (Barnard and Karaman, 1991, Bousfield, 1983, Lowry and Myers, 2017). Amphipods are highly abundant and have an important function in structuring aquatic communities (Best and Stachowicz, 2014, Duffy and Hay, 2000, González et al., 2008, Oliver et al., 1982). Furthermore, due to their omnivorous diet and intermediary trophic position, they represent a key link between trophic levels, thus playing an essential role in nutrient recycling (Dangles and Malmqvist, 2004, Machado et al., 2019, Piscart et al., 2011). The dispersal abilities of amphipods are poor due to egg brooding, lack of free-swimming larvae and extended parental care (Barnard and Karaman, 1991, Thiel, 1999, Väinölä et al., 2008). Consequently, populations can easily become genetically isolated, leading to high species diversity and biogeographical patterns which accurately reflect ancient historical events (Bauzà-Ribot et al., 2012, Copilaș-Ciocianu et al., 2019Copilaș-Ciocianu et al., 2019Copilaș-Ciocianu et al., 2019, Copilaș-Ciocianu and Petrusek, 2017Copilaș-Ciocianu and Petrusek, 2017Copilaș-Ciocianu and Petrusek, 2017, Finston et al., 2007, Hou et al., 2011). Lastly, amphipods are emerging model organisms for research on development, regeneration, ecotoxicology and evolutionary biology (Fišer, 2012, Fišer et al., 2018, Kao et al., 2016, Naumenko et al., 2017, Weston et al., 2013).

Despite global distribution, high abundance, ecological significance, and importance as emerging model organisms, only little is known about the evolutionary history of amphipods and the factors that triggered their impressive radiation. This scarcity of knowledge is due to several critical factors. Deep evolutionary relationships within the Amphipoda are uncertain. The most comprehensive phylogenetic studies were based on morphology (Lowry and Myers, 2017, Lowry and Myers, 2013), which is known to be highly homoplastic in amphipods (Berge et al., 2000). Indeed, molecular phylogenies at lower taxonomic levels do not fully agree with the morphology-based systematics (Copilaș-Ciocianu et al., 2019Copilaș-Ciocianu et al., 2019Copilaș-Ciocianu et al., 2019, Esmaeili-Rineh et al., 2015, Havermans et al., 2010, Hou and Sket, 2016, Hurt et al., 2013, Macdonald et al., 2005, Mamos et al., 2016, Verheye et al., 2016). The age of the order is puzzling as well. Bousfield, 1977, Bousfield, 1978, Schram, 1986 suggested that amphipods already appeared in the Late Palaeozoic, when the lineages of the superorder Peracarida split. Yet, unlike the rest of peracaridan orders with a pre-Cenozoic fossil record (Schram, 1986, Wolfe et al., 2016), the handful of amphipod fossil taxa are dated no earlier than Eocene and usually bear a modern appearance (Bousfield and Poinar, 1994, Coleman, 2006, Derzhavin, 1927, Kupryjanowicz and Jażdżewski, 2010). Hence, the temporal origin and main cladogenetic events of modern amphipods are not known and cannot be paralleled to main global environmental changes.

The present view on the modern diversity of amphipods can be summarised by two competing hypotheses. The first hypothesis, stating that most of the modern diversity has been attained by the end of the Palaeozoic or Early Mesozoic, is based on the current distribution of superfamilies in relationship to geochronology, cladistic relationships, or on patterns observed in related malacostracans (Barnard and Barnard, 1983, Lowry and Myers, 2013). The alternative hypothesis suggests that the diversity of amphipods could be much younger due to morphological continuity among higher taxa, and due to lower taxonomic diversity in terrestrial and deep-sea habitats in comparison to the closely related isopods (Bousfield, 1978). Molecular phylogenetic studies tend to support this view because they indicate that the onset of diversification of several major amphipod clades dates to the Cretaceous/Palaeogene (Copilaș-Ciocianu et al., 2019Copilaș-Ciocianu et al., 2019Copilaș-Ciocianu et al., 2019, Corrigan et al., 2014, Hou et al., 2014, McInerney et al., 2014, Verheye et al., 2017).

Apart from the recent fossil record and molecular timetrees, several other independent lines of evidence point out to a more recent radiation of amphipods. They are particularly cold adapted animals, exhibiting an inverse latitudinal richness gradient in marine and freshwater habitats (Barnard, 1976, Barnard and Barnard, 1983, Barnard and Karaman, 1991, Copilaș-Ciocianu et al., 2019Copilaș-Ciocianu et al., 2019Copilaș-Ciocianu et al., 2019, Rivadeneira et al., 2011, Väinölä et al., 2008), and high diversity and dominance in the cold, deep-sea benthic assemblages (Brandt, 2005, Brandt, 2000, De Broyer et al., 2004, Havermans and Smetacek, 2018, Verheye et al., 2017). This pattern is probably related to their generally low tolerance to hypoxia, given that warmer water has a lower concentration of dissolved oxygen (Modig and Ólafsson, 1998, Vaquer-Sunyer and Duarte, 2008, Wiklund and Sundelin, 2001, Wu and Or, 2005). As such, it seems unlikely that amphipods could have attained most of their current ecological disparity during the Early to Middle Mesozoic (Triassic to Early Cretaceous), a period characterized by warm temperatures even in the deep-sea (>1000 m), by weakly stratified oceans and frequent anoxic events that caused major extinctions (Jacobs and Lindberg, 2002, Lear et al., 2000, McClain and Hardy, 2010). Therefore, we hypothesize that amphipods ecologically radiated in the Late Mesozoic/Cenozoic, when large-scale continental reconfiguration induced global climatic cooling, causing the oceans to transition to a thermohaline (two-layered) circulation which, in turn, increased productivity and oxygenation levels (Donnadieu et al., 2016, McClain and Hardy, 2010, Mills et al., 2019). To test our hypothesis, we generated the first large-scale, time calibrated molecular phylogeny of the Amphipoda and reconstructed the course of diversification and ecological transitions.

Section snippets

Data collection and sequence alignment

As a taxonomic backbone for data collection we used the classification on the World Register of Marine Species database (WoRMS; http://www.marinespecies.org/) which is mainly based on Lowry and Myers (2017). All the data used in the present study is publicly available in GenBank (www.ncbi.nlm.nih.gov/genbank) and originated from 63 published and 13 unpublished studies (a list of the data sources is found in Appendix 1 and Table S1; data collection ended in January 2018). Taxa were included in a

Dataset

The phylogenetic representativeness analysis indicated a highly comprehensive taxon sampling. The Average Taxonomic Distinctiveness (AvTD) and Variation in Taxonomic Distinctiveness (VarTD) were above the highest AvTD and below the mean VarTD respectively (Fig. S1). Furthermore, von Euler’s index of imbalance (IE = 0.102) was well below the recommended 0.25 threshold value, indicating unbiased sampling (Plazzi et al., 2010) (Fig. S1).

Phylogenetic reconstruction and molecular dating

All five phylogenetic reconstruction methods yielded

Discussion

Our study reveals an ancient Permian origin of amphipods, and their delayed diversification during the Late Jurassic-Early Cretaceous followed by ecological radiation during the Cretaceous-Palaeogene. These results refute the view that most of the modern amphipod diversity already existed since the Late Palaeozoic-Early Mesozoic (Barnard and Barnard, 1983, Lowry and Myers, 2013) and help reconcile their old history with their absence in the pre-Cenozoic fossil record. Below we discuss the main

Conclusion

The Late Mesozoic is notable for its dramatic global changes which saw the rise and demise of many organismal groups, leading towards the modern biota (Alroy et al., 2008, Barba-Montoya et al., 2018, Meredith et al., 2011, Roelants et al., 2007, Schulte et al., 2010, Scott, 1995, Varga et al., 2019). In the case of the Amphipoda, these changes brought an important turning point in their evolution. The fortuitous coupling of several critical circumstances such as extinction of deep-sea

Research data

Trees and alignments are available at FigShare (doi: https://doi.org/10.6084/m9.figshare.8241401) and the Mendeley Data Platform.

Acknowledgements

We thank Dante Fenolio, David Fenwick and Alexander Semenov for kindly providing amphipod photographs. Anna Jazdzewska, Allan Myers and Cedric d'Udekem d'Acoz are thanked for their feedback. We also thank the Editor Marlise Bartholomei-Santos and two anonymous reviewers for their useful remarks. DCC was supported by the Research Council of Lithuania (09.3.3-LMT-K-712-13-0150), ŠB and CF were supported by the Slovenian Research Agency (Program P1-0184, Project N1-0069 and grant contract KB139

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