Introduction Living organisms are unicellular, composed of a single cell, or multicellular, where a group of up to ~10~(12)cells functions co-operatively (Kaiser, 2001 ). All multicellular organisms evolved from single-celled ancestors; every individual organism arises from a unicell and reproduces by forming unicells. Multicellularity enables competitive advantages, and may have shaped our oxygen-rich atmosphere (Grosberg and Strathmann, 1998 ; Kaiser, 2001 ; Schirrmeister et al., 2013 ). Multicellularity has evolved multiple times: animals, plants, algae, amoebae, fungi, and bacteria are or can all be multicellular (King, 2004 ; Grosberg and Strathmann, 2007 ; Rokas, 2008 ; Claessen et al., 2014 ). Multicellularity can be clonal (arising from division of a single cell) or aggregative (aggregation of genetically diverse cells), with clonal multicellularity considered evolutionarily more stable (Grosberg and Strathmann, 1998 ). The molecular mechanisms by which organisms become multicellular are not well understood. In this article, we outline eukaryotic multicellular evolution, and discuss how to increase our future understanding. Evolution of unicellular–multicellular transitions: a genetic toolkit for multicellularity? The most well-studied group of multicellular organisms are animals, where multicellularity likely arose once, giving rise to today's diversity of complex forms. Organisms in animal sister lineages, the aquatic “protist” choanoflagellates and filastereans (forming holozoans collectively with animals), can be unicellular or multicellular. Comparison of unicellular holozoan and animal genomes suggests that part of the “toolkit” of genes required to orchestrate multicellular development (genes for cell adhesion, cell–cell signaling and certain transcription factors) was already present in unicellular ancestors of both holozoans and animals (Abedin and King, 2008 ; King et al., 2008 ; Sebe-Pedros et al., 2011 ; Fairclough et al., 2013 ; Suga et al., 2013 ), although “metazoan-specific innovations” also exist (Suga et al., 2013 ). Data from algae extends this “common toolkit” hypothesis to other kingdoms. The Chlamydomonas (unicellular) and Volvox (simple multicellular) genomes are remarkably similar (Merchant et al., 2007 ; Prochnik et al., 2010 ), with very few species-specific genes, and expansion of Volvox extracellular matrix (ECM) gene families (Prochnik et al., 2010 ). Much is now understood about the evolutionary steps to multicellularity in Volvocine algae (Herron et al., 2009 ), but the underlying molecular–genetic mechanisms are unknown. The genome sequence of Ectocarpus , a multicellular brown alga, reveals no obvious trends of specific gene loss/gain in independent multicellular lineages (Cock et al., 2010 ). Ectocarpus contains possible integrin domains, which are important for animal development and also present in unicellular Holozoa (Cock et al., 2010 ). Ectocarpus also highlights the independent evolution of large receptor-kinase protein families as a step to drive complex multicellular evolution from a eukaryotic ancestor (Cock et al., 2010 ), as also suggested in plants (Shiu and Bleecker, 2001 ) and holozoans (Hunter and Plowman, 1997 ; Suga et al., 2014 ). Multicellular fungi possess unique non-receptor kinases (Stajich et al., 2010 ). Thus, transitions to multicellularity most likely largely require co-option of pre-existing genes, via changes in expression or regulation. Understanding unicellular–multicellular life-cycle transition mechanisms All multicellular organisms possess a unicellular life-cycle stage, undergoing a unicellular–multicellular transition in every generation. In the most complex organisms (animals and terrestrial plants), these transitions are challenging to characterize experimentally, as the unicells (gametes, zygotes) are hidden deep within host tissues (e.g., Figure 1B ). However, there are eukaryotes of varying complexity that offer tractable systems to define molecular changes underpinning unicellular–multicellular transitions, enabling new opportunities for characterization and comparison. Figure 1 Transitions between unicellular and multicellular states in plants, algae, and their relatives. (A) Simplified tree of life showing the Unikont and plant/algal lineages and their evolutionary relationships, including divergence times in millions or billions of years ago (mya or bya, respectively). Animals, choanoflagellates, filastereans, and ichthyosporeans are collectively known as holozoans (purple boxes). Plants and green algae (green boxes) together with red algae (red box) form the Archaeplastida, while brown algae are part of a separate lineage evolving from a common eukaryotic ancestor 1.6 billion years ago. (B) Highly simplified flowering plant life cycle showing unicellular–multicellular transitions (orange arrow) and multicellular–unicellular transitions (blue arrows). The multicellular seed (orange) houses the unicellular diploid zygote (
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